Eukaryotes, including plants, adapt numerous life processes to regular rhythms of light and darkness. Light and dark periods regularly alternate in a daily cycle of approximately 24 h due to the rotation of the Earth around its own axis. The duration of the light period during this 24 h day-night cycle determines the photoperiod, which varies with the season and latitude (Jackson, 2009). Plants synchronize their physiological decisions with the correct time of the year to maximize growth and to produce offspring (Casal et al., 2004). Thus, sensing of and responding to the photoperiod are important plant functions to adapt to their environment.

Among the most prominent plant responses influenced by the photoperiod are the regulation of flowering time (Carré, 2001; Song et al., 2015), tuberization (Sarkar, 2010), bud setting, and dormancy (Jackson, 2009; Singh et al., 2017). In annual plants, senescence is adjusted by the photoperiod (Serrano-Bueno et al., 2021) and in perennial plants like trees, the growth cessation is influenced by season-dependent photoperiods (Singh et al., 2017). In temperate climate zones but also in tropical regions, the photoperiod is the dominant environmental factor controlling the onset and end of the seasonal growing (Adole et al., 2019). Scent emission from flowers is also under the control of the photoperiod (Hendel-Rahmanim et al., 2007) to mention just a few examples of photoperiod-regulated developmental processes in plants.

Based on their flowering response to the photoperiod, plants can be classified into three groups: short-day, long-day, and day-neutral plants. This classification is based on the critical day length (CDL), which determines the ability of plants to respond to the photoperiod. Short-day-grown plants flower when the photoperiod is shorter than the CDL, while long-day plants flower only, when the photoperiod is longer than the CDL. Day-neutral plants do not respond to the photoperiod (Jackson, 2009). Besides the CDL, the plant developmental phase determines the ability to sense and subsequently respond to photoperiods. The flowering response of Arabidopsis plants is insensitive to photoperiods during their juvenile phase. Entering the adult phase makes Arabidopsis sensitive to photoperiods enabling responses to floral inducers (Matsoukas, 2014). Taken together, the synchronization of the photoperiod sensing and intrinsic developmental programs or developmental phases with the seasonal photoperiod is essential for the reproduction and survival of plants.

Photoperiod sensing not only enables plants to synchronize their developmental processes with a specific time of the year but also alleviates the impact of environmental stresses occurring at the same time every year. Recently, the interest in the effect of the photoperiod on the response to abiotic and biotic stresses has grown. For example, the role of shortening of days in cold acclimation to prepare for freezing winter temperatures has been uncovered (Ouellet and Charron, 2013). The photoperiod has also been shown to influence the plants’ resistance to drought stress (Iuchi et al., 2001; Han et al., 2013a) and salt stress (Kim et al., 2013; Park et al., 2016). In addition, increasing evidence suggests that the length of the light period is important for the outcome of plant-pathogen interactions (e.g., Griebel and Zeier, 2008). Thus, photoperiod sensing enables plants to improve their responses to diverse environmental stresses (Figure 1). However, sudden changes in the photoperiod can also result in stress. Although the molecular mechanisms underlying this new abiotic stress form are not yet completely resolved (Nitschke et al., 2016, 2017; Abuelsoud et al., 2020; Frank et al., 2020), experiments revealed that changes in the photoperiod elicit stress reactions in Arabidopsis plants, which resemble responses to pathogen attack (Cortleven et al., 2021). The establishment of systemic acquired resistance (SAR) in plants forms an important defense against future pathogen attacks (Conrath et al., 2006). As photoperiod stress provokes similar effects, this might open new horizons for the use of altered photoperiods as a sustainable tool to alleviate pathogen infections and thereby decrease yield losses in horticulture. In the following chapters, we will address the above-mentioned topics in more detail.

The perception of and response to photoperiods in plants require a sensing mechanism, which involves the detection of light (via photoreceptors or chloroplasts) and the measurement of time (via the circadian clock) (Jackson, 2009; Serrano-Bueno et al., 2021).

Light perception by photoreceptors and chloroplasts provides plants with comprehensive information concerning their surrounding light environment, such as quality (spectral composition, direction), quantity, intensity, and duration of incoming irradiation (Figure 1). In Arabidopsis thaliana, five photoreceptor families sense the light from different parts of the solar light spectrum: red/far-red light is detected by phytochromes (phyA to phyE). Blue light is perceived by cryptochromes (CRY1, CRY2, CRY3), phototropins (PHOT1, PHOT2), and F-box containing flavin-binding proteins ZEITLUPE (ZTL) and FLAVIN-BINDING KELCH REPEAT F-BOX1 (FKF1)/LOV KELCH PROTEIN2 (LKP2). UV light is sensed by the UVR8 photoreceptor (for review, see Sanchez et al., 2020; Roeber et al., 2021). All of the above-mentioned photoreceptor families are involved in the light entrainment of the circadian clock.

Besides the photoreceptors, chloroplasts operate as plant light sensors and respond to different photoperiods by altering their ultrastructure (Lepisto and Rintamaki, 2012). Chloroplasts of plants grown under long days exhibit smaller grana stacks and increased chlorophyll content. These features correspond to structural and photosynthetic characteristics typical of sun plants (Walters and Horton, 1995). Redox signals arising from chloroplasts determine the light intensity-dependent acclimation of plants (Pfannschmidt et al., 2009). Which signaling mechanisms are involved in the photoperiodic-dependent development of chloroplasts remains to be resolved. The redox state of the photosynthetic electron transport chain, ROS metabolism, and chloroplast-to-nucleus retrograde signaling are only few examples of possible pathways involved, all acting independent of the photoreceptors (for review, see Lepisto and Rintamaki, 2012; Feng et al., 2016). Besides the chloroplast ultrastructure, the photoperiod regulates the photosynthate partitioning to starch and the amount of carbohydrate (C) stored in chloroplasts (Zeeman et al., 2007). Under conditions where less C is available such as short photoperiods, a larger proportion of the fixed C is allocated into starch (Smith and Stitt, 2007). During the night the near-linear starch degradation is slowed down as compared to long-day-grown plants. This results in an almost but not completely exhausted starch content at dawn preventing C-starvation or C-excess at the end of the night period (Stitt and Zeeman, 2012; Moraes et al., 2019). This pattern of C-mobilization is robust across different photoperiods (Stitt and Zeeman, 2012; Moraes et al., 2019). Also here, the exact molecular mechanisms controlling the formation of starch under various photoperiods are not known, but possible feedback inhibition from the carbohydrate metabolism, redox regulation, transcriptional control of chloroplast enzymes, and circadian regulation might play a role.

The circadian clock enables plants to measure time by an endogenous time-keeping mechanism (Hsu and Harmer, 2014; Figure 2). The clock is set through daily entrainment, especially by light and temperature, in order to adjust the internal rhythm (McClung, 2006). In Arabidopsis thaliana, the circadian clock consists of multiple interlocked transcription-translation feedback loops (Hsu and Harmer, 2014). The MYB-domain transcription factor genes CIRCADIAN CLOCK ASSOCIATED1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) are expressed in the morning (Schaffer et al., 1998; Wang and Tobin, 1998) and repress the expression of TIMING OF CAB EXPRESSION1 (TOC1) during the day (Alabadi et al., 2001). In turn, TOC1 represses the transcription of CCA1 and LHY (Gendron et al., 2012). Late at night, TOC1 transcription is down-regulated by an Evening Complex (EC), which is composed of three proteins: EARLY FLOWERING3 (ELF3), ELF4, and LUX ARRHYTHMO (LUX). This down-regulation enables transcription of LHY and CCA1 to resume the following dawn. PSEUDO-RESPONSE REGULATOR9 (PRR9), PRR7, and PRR5 are expressed in consecutive waves throughout the day and repress CCA1 and LHY expression (Nakamichi et al., 2012). Additional rhythmically expressed transcriptional activators, such as REVEILLE4 (RVE4), RVE6, and RVE8, the LIGHT-REGULATED WD1 (LWD1) and LWD2 proteins, and the transcription factors NIGHT LIGHT-INDUCIBLE AND CLOCK-REGULATED GENE1 (LNK1) and LNK2 also contribute to the clock function (Rawat et al., 2011; Rugnone et al., 2013). The circadian clock contributes to the plants’ ability to respond to various environmental stresses but there is also a reciprocal influence of abiotic stresses on the clock function. More information about this can be found in the reviews of Sanchez et al. (2011), Kiełbowicz-Matuk and Czarnecka (2014), Grundy et al. (2015), Seo and Mas (2015), and Sharma et al. (2021). A novel webtool to investigate the transcriptional networks regulated by light and the circadian clock has been launched recently (de los Reyes et al., 2020). With ATTRACTOR (Arabidopsis Thaliana TRanscriptionAl Circadian neTwORk¹), target genes of circadian regulators can be identified. This might contribute to a better understanding of the interaction between the circadian clock and plant responses to environmental stresses.

One of the circadian clock-controlled genes that have a crucial role in the photoperiod sensing mechanism is GIGANTEA (GI) (Fowler et al., 1999). It encodes a large single-gene encoded protein with a chaperone activity (Cha et al., 2017). Upon blue light perception, the stability of the F-box protein ZEITLUPE (ZTL) improves due to interaction with GI. ZTL is an evening-phased E3 ubiquitin ligase targeting the clock components TOC1 and PRR5 for proteasomal degradation (Mas et al., 2003; Kiba et al., 2007). GI protein abundance peaks in the evening, thereby maintaining ZTL abundance high. Consequently, high amplitude oscillations of TOC1 and PRR5 are sustained (Kim et al., 2007). This reinforces the entrainment of the clock resulting in the correct setting of the phase of clock output genes such as CONSTANS (CO), encoding a central protein in photoperiod-dependent flowering (Suarez-Lopez et al., 2001; Shim et al., 2017). GI also interacts with FKF1 upon blue light perception causing the degradation of CYCLING DOF FACTOR1 (CDF1), which is a transcriptional repressor of CO (Figure 2; Sawa et al., 2007). The synchronization of the correct timing of protein stabilization during long days with the circadian-regulated expression of FKF1, GI, and CDF1 is essential for photoperiodic responses, such as flowering. Interesting to mention is that the CO-FT-GI-CDF hub is conserved among distantly related flowering plants (Serrano-Bueno et al., 2021).

GI also regulates the maturation of miR172 (Jung et al., 2007), which targets APETALA2 (AP2) and the AP2-like genes TARGET OF EAT1 (TOE1), TOE2, TOE3, SCHLAFMÜTZE (SMZ), and SCHNARCHZAPFEN (SNZ) (Figure 2). The miR172-mediated posttranscriptional downregulation of these floral repressors regulates flowering time and floral development in the shoot apical meristem (Mathieu et al., 2009) depending on the age of the plants (Aukerman and Sakai, 2003). In addition, GI controls the circadian clock-mediated photoperiod sensing together with EARLY FLOWERING3 (ELF3). In their absence, the circadian clock fails to properly respond to light signals, resulting in the breakdown of the photoperiod sensing mechanism (Anwer et al., 2020).

GI plays not only a central role in the photoperiod sensing mechanism but is also involved in mediating the impact of the photoperiod in response to diverse stresses (Figure 2), e.g., drought, oxidative, osmotic, and cold stress (Cao et al., 2005; Fornara et al., 2015), as will be outlined further below.

A possible reason for the impact of the photoperiod on responses to diverse stresses is its regulatory influence on the plant redox state (for review see Shim and Imaizumi, 2015). The plant redox state and regulation of redox reactions are connected with levels of reactive oxygen species (ROS). ROS have previously been considered only as toxic by-products of aerobic metabolism, but recent research highlights their importance as plant signaling molecules (for review see Mittler, 2017). In addition, ROS cause post-translational modifications of cysteine residues in redox-sensitive proteins and thus interfere with the redox regulatory network of the cell allowing fast responses of plants to environmental cues (Cejudo et al., 2021).

ROS include several oxygen-containing molecules, such as singlet oxygen (¹O₂), superoxide (O₂^–), hydroxyl radicals (OH^–), and hydrogen peroxide (H₂O₂) (Shim and Imaizumi, 2015; Mittler, 2017). Of these, especially H₂O₂ levels are regulated by the photoperiod. In the algae Chlamydomonas reinhardtii, elevated H₂O₂ levels in the presence of light result from slower H₂O₂ degradation due to light-dependent inactivation of catalases (Shao et al., 2008). Similar observations were made in rye (Secale cereale) leaves (Hertwig et al., 1992).

Experiments with Arabidopsis catalase2 (cat2) mutants exposed to different day lengths were particularly informative about the influence of the photoperiod on oxidative stress responses. The photoperiod, in which the cat2 mutants are grown, is decisive for the oxidative stress response and regulates H₂O₂-induced gene expression as well as the severity of the cell death phenotype (Queval et al., 2007; Chaouch et al., 2010; Shim and Imaizumi, 2015). While short-day-grown cat2 mutants do not display any lesions, lesion formation is visible in long day-grown cat2 mutants pointing to elevated H₂O₂ levels. Further analysis revealed that increased peroxisomal H₂O₂ in cat2 triggers pathogen defense responses and enhances the plants’ resistance in a photoperiod-dependent manner. Also lesion simulating disease1 (lsd1) mutants formed lesions only in long photoperiods (Mateo et al., 2004; Shim and Imaizumi, 2015). LSD1 is a catalase-interacting protein, regulating catalase activity, as a consequence, catalase activity is decreased in lsd1 mutants. LSD1 and CATALASE genes interact genetically and their encoded proteins are part of a protein complex, which plays an important role in regulating programmed cell death (PCD) (Li et al., 2013).

Similar as observed for catalase, also other enzymes involved in ROS detoxification including ascorbate peroxidase and NAD-malate dehydrogenase showed in Arabidopsis a higher activity under long photoperiods (Becker et al., 2006). GI was shown to be a negative regulator of the expression of genes encoding enzymes detoxifying ROS. Indeed, the increased tolerance of gi-3 mutants to oxidative stress is caused by the constitutive activation of SUPEROXIDE DISMUTASE (SOD) and ASCORBATE PEROXIDASE (APX) genes (Cao et al., 2006).

Together these publications support a photoperiod-dependent regulation of the plant redox state. Photoperiod sensing is linked to redox regulation, allowing efficient light usage and redox balancing in short days and preventing oxidative damage in long days (Becker et al., 2006). Especially catalases but also SOD and APX seem to be important factors exerting photoperiod information on redox regulation (Shim and Imaizumi, 2015).

Sudden changes in the photoperiod, in particular its prolongation, cause photoperiod stress in short-day-adapted A. thaliana plants (Nitschke et al., 2016, 2017; Figure 4). The photoperiod stress response, which was originally observed after a prolongation of the light period by 24 h, is characterized by a typical course of events: During the night following an extended light period, the expression of stress marker genes, such as ZINC FINGER of ARABIDOPSIS THALIANA12 (ZAT12) and BON ASSOCIATED PROTEIN1 (BAP1), is induced, the concentration of the stress hormones JA and SA increase and oxidative stress occurs. The nightly increase in oxidative stress coincides with a strong decrease in the ascorbic acid (ASC) redox state and the formation of peroxides. The peroxide formation is associated with an increase of PEROXIDASE (PRX) gene expression as well as enhanced PRX and decreased catalase activities (Abuelsoud et al., 2020). During the next day, the photosystem II maximum quantum efficiency decreases, and eventually PCD ensues in the leaves (Nitschke et al., 2016, 2017).

Photoperiod stress was first noted in cytokinin (CK)-deficient Arabidopsis plants, which show a particularly strong stress response. Among the CKs, especially trans-zeatin has a protective function acting through the ARABIDOPSIS HISTIDINE KINASE3 (AHK3) receptor and the transcriptional regulators ARABIDOPSIS RESPONSE REGULATOR2 (ARR2), ARR10, and ARR12 (Figure 4; Frank et al., 2020). Certain clock mutants (e.g., cca1 lhy, elf3) also show a stronger molecular and phenotypical response to sudden prolongations of the photoperiod. Both photoperiod stress-sensitive clock mutants and CK-deficient plants have a lower expression or impaired function of CCA1 and LHY, two key regulators of the circadian clock. This indicates that a functional clock is required to cope with photoperiod stress (Figure 4; Nitschke et al., 2016, 2017).

In short-day-entrained Arabidopsis plants, a prolongation of the light period by only 4 h is sufficient to induce the production of ROS and the expression of stress marker genes during the following night. Longer prolongations of the light phase induce a gradually stronger stress response, which indicates that light duration has an impact on the strength of the photoperiod stress response (Abuelsoud et al., 2020). Shorter prolongations of the light period, which cause lower stress levels, are perceived as not harmful and may present a beneficial stress (eustress), while higher stress levels (by longer prolongations) induce a true stress (distress) (Krasensky-Wrzaczek and Kangasjarvi, 2018).

RNA-seq analysis of 5-weeks-old short-day grown Arabidopsis plants exposed to a 24 h-prolongation of the light period revealed that photoperiod stress causes massive time-dependent transcriptomic changes during the night following the prolonged light period (Cortleven et al., 2021). Among the photoperiod stress-responsive genes are numerous genes related to ROS. The photoperiod stress transcript profile resembles that caused by ozone stress and pathogen attacks, which commonly elicit an apoplastic oxidative burst. Moreover, both SA and camalexin levels increased and transcript levels of genes involved in SA biosynthesis, such as ISOCHORISMATE SYNTHASE1 (ICS1), and genes involved in SAR, such as PATHOGENESIS RELATED1 (PR1) were induced by photoperiod stress (Cortleven et al., 2021).

Interestingly, photoperiod stress pre-treated wild-type plants showed less P. syringae pv. tomato DC3000 colony-forming units after infection in comparison to non-photoperiod stress-treated plants. This indicates that not only similar molecular pathways are activated in response to photoperiod stress and pathogen attack, but that photoperiod stress pre-treatment leads to improved pathogen immunity in Arabidopsis plants without an actual pathogen attack (Cortleven et al., 2021). Other reports support this conclusion. In tomato, it was shown that nightly red light treatment improved the resistance against P. syringae pv. tomato DC3000 (Yang et al., 2015). The improved resistance was associated with increased SA levels and the induction of defense-related genes, which is typical of a photoperiod stress response (Cortleven et al., 2021). The transfer of short-day-grown Arabidopsis plants to long-day conditions, causing essentially photoperiod stress by 8 h light prolongation, resulted in an improved resistance against B. cinerea (Cagnola et al., 2018). Prolonged light exposure due to transfer from short to long days resulted in lower nuclear abundance of CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1), thereby leading to stabilization of DELLA proteins and increased expression of the JA-signaling gene JASMONATE INSENSITIVE1 (MYC2) (Cagnola et al., 2018). Exposure of maize to a prolonged light period increased resistance against C. carbonum race 1 (Marla et al., 2018). These studies indicate that the response to photoperiod stress is conserved among different plant species and that it has similar effects on pathogen resistance. Future research needs to identify the specific mechanisms conferring the improved pathogen resistance in photoperiod stress-treated plants.

The photoperiod provides plants with information to synchronize their developmental program with the prevailing season. It is used to match the optimal conditions for offspring production and to alleviate the threats of seasonal stresses occurring at the same time every year. In this review, we have summarized the complex photoperiod sensing mechanisms (Figures 1, 2) and especially focussed on the role of the photoperiod in plant responses to cold, drought, osmotic and biotic stresses (Figure 3 and Table 1). While the molecular mechanisms of photoperiod-dependent regulation of cold, drought, and osmotic stress are at least partly elucidated, the impact of the photoperiod on biotic stress responses remains descriptive.

Recent studies (Nitschke et al., 2016, 2017) revealed that a sudden prolongation of the photoperiod causes a new form of abiotic stress, namely photoperiod stress, resulting in a nightly ROS accumulation in the apoplast and a stress response resembling pathogen infection (Abuelsoud et al., 2020; Cortleven et al., 2021). Photoperiod stress signals might have an adaptive value, for example by acting as a priming agent, which improves the plants’ performance to future stresses. The ecological relevance of photoperiod stress needs to be unveiled. It has been hypothesized that changes in intensity and ratios of wavelength during dawn and dusk that depend on weather conditions may modulate the output of the photoperiod sensing system (Abuelsoud et al., 2020), but the experimental proof is missing.

In view of the impact of the photoperiod on plant responses to pathogens, it may be envisaged that controlled changes of the photoperiod have a perspective for application in greenhouse farming. In these controlled environmental conditions the duration, intensity and wavelength composition of the illumination can be precisely regulated by light-emitting diodes (LEDs), which holds the potential to improve crop yield and quality (Jones, 2018; Lazzarin et al., 2021). LEDs can also be used for pest management. Several studies showed the influence of the light environment in greenhouses (including the length of the photoperiod and light quality) (for review, see Gallé et al., 2021; Lazzarin et al., 2021), on plant resilience against pathogens such as B. cinerea in strawberries (Meng et al., 2020) or tomatoes (Yang et al., 2015). Understanding how supplemental light through LEDs acts on plant growth and defense may lead to novel sustainable horticultural methods for pest management.

VR and AC wrote the draft of the manuscript. VR, AC, and TS revised the manuscript. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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