Plants have a tendency to flower if placed under unsuitable growth conditions. A review of the literature reporting such non-photoperiodic flowering indicated that most of the factors responsible for flowering could be regarded as stress. Those stress factors include poor nutrition, high or low temperature, high- or low-intensity light, ultraviolet light and many others. This flowering would be called stress-induced flowering. The plants induced to flower by stress produced fertile seeds, and the progeny developed normally in Pharbitis nil and Perilla frutescens var. crispa. Grafting experiments using two varieties of P. nil revealed that a transmissible flowering stimulus is involved in stress-induced flowering. Salicylic acid and/or the flowering gene FLOWERING LOCUS T may be involved in the stress-induced flowering of P. nil, P. frutescens, Arabidopsis thaliana and Lemna paucicostata. The stressed plants do not need to await the arrival of a season when photoperiodic conditions are suitable for flowering, and such precocious flowering might assist in species preservation. Thus, stress-induced flowering might have a biological benefit and should be considered as important as photoperiodic flowering and vernalization.
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Flowering is regulated by both endogenous and environmental factors. One endogenous factor is the autonomous pathway of flowering regulation in Arabidopsis thaliana (Simpson 2004). Day-neutral plants switch from vegetative to reproductive growth in response to endogenous signals after a certain period of time (McDaniel 1996). Environmental factors that regulate flowering include the duration of the day and night periods in photoperiodic flowering and temperature in vernalization (Thomas and Vince-Prue 1997). Flowering that cannot be classified into these categories has also been sporadically reported. Some plants for which flowering is basically regulated photoperiodically flowered under unsuitable photoperiodic conditions when grown under certain conditions. Experienced flowering physiologists have noticed that plants have a tendency to flower if placed under unsuitable growth conditions. However, such unusual flowering has not been studied systematically. We surveyed the flowering behavior reported in the literature and analyzed the non-photoperiodic flowering responses in some plant species. We concluded that many cases of non-photoperiodic flowering are induced by stress. Stress is as important a flower-inducing factor as night length and low temperature.
History of the study of stress-induced flowering
The short-day plant Pharbitis nil (synonym Ipomoea nil) can flower under long days when grown in tap water (poor-nutrition conditions), at 12 to 15â„ƒ (low-temperature conditions) or under 15,000 to 20,000 lux light (high-intensity light conditions) (Shinozaki and Takimoto 1982; Shinozaki et al.1982, 1988a, b, 1994; Shinozaki 1985; Swe et al.1985; Hirai et al.1993, 1994, 1995). These flowering responses were mainly studied by Dr. M. Shinozaki and his coworkers at Kyoto University, Japan, who called such flowering "long-day flowering".
The responses to these conditions differ depending on the cultivar (Swe et al. 1985). The most common cultivar (cv.), Violet, responded to all these conditions and flowered, whereas cv. Tendan and Kidachi were not induced to flower by poor nutrition or high-intensity light. Kidachi and the white-flowered mutant of Violet responded more sensitively to low-temperature than did wild-type Violet (Ishimaru et al. 1996). Chlorogenic acid (CGA) and some other phenylpropanoids were found to accumulate in the cotyledons during the treatments with poor nutrition, low temperature or high-intensity light (Shinozaki et al. 1988a, b, 1994, Hirai et al. 1993, 1994). Many reports indicated a close correlation between CGA content and flowering response (Ishimaru et al. 1996), in which the number of flower buds increased in parallel with the CGA content. Kidachi that was not induced to flower by poor nutrition or high-intensity light did not accumulate CGA under these conditions. A white-flowered mutant of Violet responded to low temperature more sensitively and accumulated more CGA than did the wild type. Further, the flowering induced by these conditions was accompanied by an increase in phenylalanine ammonia-lyase (PAL) activity (Hirai et al. 1995). Aminooxyacetic acid (AOA) inhibited flowering (Shinozaki et al. 1988a, 1994, Hatayama and Takeno 2003). AOA inhibits the activity of PAL, which catalyzes the conversion of phenylalanine to t-cinnamic acid to result in the accumulation of CGA. These findings suggested that endogenous CGA may be involved in long-day flowering. However, exogenous application of CGA could not induce flowering (Shinozaki et al. 1988a, 1994, Ishimaru et al. 1996).
Long-day flowering may be caused by stress
Although the factors that can induce long-day flowering are not related each other, PAL is involved in flowering induced by any of these conditions. This suggests that these factors may stimulate flowering through a common signal transduction pathway. Poor nutrition, low temperature and high-intensity light can be regarded as stress factors, and PAL activity increases under stress conditions (Dixon and Paiva 1995). Accordingly, we predicted that long-day flowering might be induced by stress.
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We found that non-photoperiodic flowering is not restricted to P. nil. We observed that the short-day plant Lemna paucicostata flowered under long-day conditions and the long-day plant Lemna gibba flowered under short-day conditions when they were grown in tap water, i.e. under poor nutrition conditions (unpublished data). Further, we found that the short-day plant Perilla frutescens var. crispa flowered under long-day conditions when grown under low-intensity light (Wada et al 2010b). Low-intensity light can be also regarded as stress factor.
We have noticed that non-photoperiodic flowering has been sporadically reported. Accordingly, we surveyed past studies and found that many of the conditions under which flowering was induced can be considered to be stress conditions (Wada and Takeno 2010). Some examples of them are listed in Table 1. Flowering has been induced by high- and low-intensity light, ultraviolet-C light, drought, poor nutrition, high and low temperature and mechanical stimulation. These factors can be regarded as stress, although many of those reports did not mention that stress was responsible for flowering. Papers that clearly mentioned that flowering was induced by stress have appeared only recently (Hatayama and Takeno 2003; Martínez et al. 2004; Kolár and Senková 2008).
Stress can be simply defined as a situation in which the vegetative growth of plants is suppressed. Flowering is the change from vegetative growth to reproductive growth. Therefore, it is quite natural that flowering is accelerated by the suppression of vegetative growth by stress. Plants can modify their development to adapt to stress conditions. Stressed plants may flower to produce the next generation as an emergency response. In this way, plants can preserve the species even in an unfavorable environment. This idea is supported by the recent change in the understanding of shade avoidance responses. The most typical phenotype of the shade avoidance response is rapid stem elongation, but recent articles report that an important component of the shade avoidance syndrome is an acceleration of flowering observable in all shade-avoiding plants (Adams et al. 2009). Accelerated flowering and seed production under unfavorable environments increases the probability of the survival of the individual and therefore of the species. This is true also in flowering induced under stress conditions.
Thus, it is reasonable to assume that stress can induce flowering, and the evidence for this is accumulating (Table 1). Therefore, we called such flowering "stress-induced flowering" (Hatayama and Takeno 2003; Wada et al. 2010a, b, Wada and Takeno 2010).
Case studies of stress-induced flowering
P. nil, cv. Violet was induced to flower when grown in a diluted mineral nutrient solution or tap water for 20 days under long-day conditions (Wada et al. 2010a). The vegetative growth of the plants under these poor-nutrition conditions was substantially inhibited. Because the suppression of vegetative growth indicated that the plants were stressed, this flowering can be considered stress-induced flowering. The flowering response was weaker under the weaker stress condition (1/10-strength nutrient solution) than under the stronger stress condition (1/100-strength nutrient solution). The other cultivar, Tendan, was not induced to flower even when grown in tap water, although vegetative growth was inhibited. Thus, nutrient stress does not induce flowering in all cultivars. Flowering of the white-flowered mutant of Violet was induced by a low temperature stress treatment of 13 Â°C for 10 days, whereas the control plants kept at 25 Â°C remained vegetative (Hatayama and Takeno 2003).
The Violet plants induced to flower by poor-nutrition stress produced fertile seeds, and their progeny developed normally (Wada et al. 2010a). Defoliated Violet scions grafted onto rootstocks of Violet or Tendan were induced to flower under poor-nutrition stress conditions. This result indicates that a transmissible flowering stimulus is involved in the induction of flowering by poor-nutrition stress. The poor-nutrition stress-induced flowering and cold-stress-induced flowering were inhibited by AOA, which is an inhibitor of PAL, and this inhibition was almost completely reversed by benzoic acid or salicylic acid (SA) (Hatayama and Takeno 2003; Wada et al. 2010a). However, exogenously applied SA did not induce flowering under non-stress conditions, suggesting that SA may be necessary but not sufficient to induce flowering. PnFT2, a P. nil ortholog of the flowering gene FLOWERING LOCUS T (FT) of A. thaliana, was expressed when the Violet plants were induced to flower by growing in tap water. However, the expression of PnFT1, another ortholog of FT, was not induced, suggesting a specific involvement of PnFT2 in stress-induced flowering (Wada et al. 2010a).
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The short-day plant Perilla frutescens var. crispa was induced to flower under long-day conditions when grown under low-intensity light (Wada et al. 2010b). Two forms of P. frutescens were planted in vermiculite when the cotyledons had expanded and were grown under long-day conditions with different light intensities. All of the red-leaved plants grown under 30 Âµmol m-2 s-1 flowered, whereas the plants grown under 60 or 120 Âµmol m-2 s-1 did not. The green-leaved form was also induced to flower under 30 Âµmol m-2 s-1, although the flowering response was lower than that of the red-leaved form. Flowering under low-intensity light accompanied a reduction in stem length. The reduction of vegetative growth results from stress, and therefore, the flowering of P. frutescens under low-intensity light is another example of stress-induced flowering. P. frutescens is an obligatory short-day plant (Jacobs 1982) that does not have a vernalization requirement. Therefore, the flowering under long-day conditions found in this study is independent of photoperiodism and vernalization. Photosynthetic activity may have decreased under low-intensity light conditions. However, it is unlikely that the photosynthetic deficiency induced flowering because the photoassimilate is a flower-inducing factor (Bernier and Périlleux 2005). In fact, sucrose induced flowering of P. frutescens cultured in vitro under long-day conditions (Purse 1984). Generally, plants grown under low-intensity light conditions are etiolated and elongated (Lorrains et al. 2008). However, the stem length of P. frutescens was shortened, and the leaves became green under low-intensity light. Therefore, the response of P. frutescens to low-intensity light was different from the general photomorphogenetic response or shade avoidance response. P. frutescens is reportedly induced to flower by poor nutrition (Wada and Totsuka 1982) or low temperature (Zeevaart 1969). Accordingly, the red-leaved P. frutescens was treated with several stress factors other than low-intensity light. The plants were grown in tap water or a diluted mineral nutrient solution (poor-nutrition stress), at 5 to 15°C (low-temperature stress), with 50 to 400 mM NaCl (salt stress) or with poor watering (water stress). None of these factors induced flowering, even though they retarded vegetative growth. This indicates that not all kinds of stress can induce flowering. Although high-intensity light has been well studied as a stress factor (Chalker-Scott 1999), there are only a few reports on low-intensity light as a stress factor. Red-leaved P. frutescens (De Zeeuw 1953, Gaillochet et al. 1962), Lemna perpusilla (Takimoto 1973) and A. thaliana (Smith and Whitelam 1997) flowered under low-intensity light.
The red-leaved P. frutescens that were exposed to low-intensity light when their cotyledons had just expanded were induced to flower by the 3-week treatment, and 100% flowering occurred after the 4-week treatment (Wada et al. 2010b). Flowers were formed even at the cotyledonal nodes. Prolonged treatment for 5 weeks did not increase the number of flowers or inflorescences. The plants could respond to low-intensity light immediately after the cotyledons had expanded. The flowering response decreased with an increase in plant age, and flowering was not induced when the low-intensity light treatment began 2 weeks after the cotyledons had expanded or at any later time. Treatment for at least 3 weeks was required to induce flowering. The low-intensity light stress-induced flowering was inhibited by PAL inhibitors.
Ultraviolet (UV)-C light stress promoted flowering in A. thaliana (Martínez et al. 2004). The other stresses of extreme temperature, water deficiency or high light irradiation did not accelerate flowering. UV-C irradiation accelerated flowering in wild-type Columbia (Col) ecotype in a dose-dependent manner between 0 and 200 mJ cm-2. UV-C irradiation of the same dosage did not promote flowering of the nahG transgenic plants that are expressing bacterial salicylate hydroxylase and are unable to accumulate SA because of the rapid and efficient conversion of SA to catechol. UV-C irradiation increased expression of the SA-responsive PR1 gene and the gene encoding the SA biosynthetic enzyme in Col. Exogenously applied SA accelerated flowering of Col, but the nahG plants were not responsive to SA treatment. UV-C induced expression of the flowering gene FT and moderately induced CONSTANS (CO) expression in wild type. None of these genes were induced by UV-C in nahG plants. Flowering promoted by SA requires the reduced expression of FLC and enhanced expression of FT .
Poor-nutrition conditions accelerated the flowering of A. thaliana (Kolár and Senková 2008). The authors suggested that this precocious flowering was due to stress. When plants were grown in a full-strength nutrient solution for 3 to 5 weeks and then transferred to a 1/10- to 1/1000-strength media, the time to flower was notably shortened. The accelerating effect was stronger when the stress was applied earlier, and the more diluted solution caused greater acceleration. This acceleration was more pronounced in short-day conditions than in long-day conditions. The response was stronger in the ecotype Landsberg erecta (Ler) than in Col. The nutrient-deficient Ler plants formed normal flowers and fruits with seeds. On the other hand, Marín et al. (2010) reported that flowering of A. thaliana was more rapid under low nitrate conditions, although low nitrate did not act via a general stress pathway. They intended to study the specific effect of nitrate on flowering, and therefore added glutamine to the medium as a constitutive nitrogen supply together with nitrate of varied concentrations. The plants that flowered earlier on low nitrate media showed similar growth rates to the plants grown on high nitrate media. ã€€
General stress leads to early flowering in A. thaliana. High-intensity light of 800 Âµmol m-2 s-1, high temperature of 26 Â°C, photochilling of 800 Âµmol m-2 s-1 at 16Â°C or continuous light treatments lead to earlier flowering in wild type Ler, but not in the fca1 co-2 ga1-3 triple mutant (Marín et al. 2010).
When the short-day plant L. paucicostata strain 6746 was cultured in tap water under non-inductive long-day conditions, the multiplication of fronds decreased and flowering occurred (Shimakawa 2011). Thus, poor nutrition conditions functioned as a stress factor, and this stress induced flowering. The poor nutrition stress-induced flowering response was weaker than that induced by short-day treatment. L-2-aminooxy-3-phenylpropionic acid (AOPP), an inhibitor of PAL, inhibited the poor nutrition stress-induced flowering without preventing the vegetative growth. More SA was detected in the flowered plants than in the control plants. The results suggest the involvement of SA in the stress-induced flowering of L. paucicostata. Exogenously applied SA is known to induce flowering in L. paucicostata and L. gibba (Cleland and Ajami 1974; Cleland and Tanaka 1979; Cleland et al. 1982). However, SA is not considered to be an endogenous flower-regulating factor because the endogenous SA level is not altered by photoperiodic conditions (Fujioka et al. 1983). It is possible that SA is the endogenous flower-regulating factor in stress-induced flowering but not in photoperiodic flowering.
Nitrogen deficiency was reported to induce flowering in L. paucicostata in long-day conditions (Tanaka et al. 1988, 1989, 1991). This day length-independent flowering occurred in media supplemented with inorganic salts other than nitrogen, and therefore, it is not certain whether this is a kind of poor nutrition stress-induced flowering. Nitrogen deficiency does not always function as stress as mentioned above for A. thaliana.