|II.||Effects of elevated [CO2] on flowering time||245|
|III.||Mechanisms for altered flowering time in response to elevated [CO2]||250|
|II.||Effects of elevated [CO2] on flowering time||245|
|III.||Mechanisms for altered flowering time in response to elevated [CO2]||250|
Flowering is a critical milestone in the life cycle of plants, and changes in the timing of flowering may alter processes at the species, community and ecosystem levels. Therefore understanding flowering-time responses to global change drivers, such as elevated atmospheric carbon dioxide concentrations, [CO2], is necessary to predict the impacts of global change on natural and agricultural ecosystems. Here we summarize the results of 60 studies reporting flowering-time responses (defined as the time to first visible flower) of both crop and wild species at elevated [CO2]. These studies suggest that elevated [CO2] will influence flowering time in the future. In addition, interactions between elevated [CO2] and other global change factors may further complicate our ability to predict changes in flowering time. One approach to overcoming this problem is to elucidate the primary mechanisms that control flowering-time responses to elevated [CO2]. Unfortunately, the mechanisms controlling these responses are not known. However, past work has indicated that carbon metabolism exerts partial control on flowering time, and therefore may be involved in elevated [CO2]-induced changes in flowering time. This review also indicates the need for more studies addressing the effects of global change drivers on developmental processes in plants.
Over the past three decades, a large number of studies have focused on the effects of increasing atmospheric carbon dioxide concentrations, [CO2], on the physiology, growth and reproduction of plants. There are three main reasons for such a large investment in CO2 plant research: atmospheric CO2 directly affects plant physiology and growth by serving as a primary substrate for photosynthesis; plants may act as sinks for CO2 emitted through fossil fuel combustion; and, unlike other global change factors such as temperature and precipitation that vary on a regional scale, atmospheric [CO2] is increasing at a similar rate on a global scale (Tans et al., 1990). Plants grown at elevated [CO2], especially those utilizing the C3 photosynthetic pathway, often exhibit marked changes in both physiological functioning and growth relative to plants grown at the current [CO2] value (for reviews see Ceulemans & Mousseau, 1994; Gunderson & Wullschleger, 1994; Amthor, 1995; Curtis, 1996; Drake et al., 1997; Curtis & Wang, 1998; Ward & Strain, 1999; Poorter & Navas, 2003; Long et al., 2004; Ainsworth & Long, 2005). Generally, plants display increased growth at elevated [CO2] that is associated with lower transpiration and increased photosynthesis. This enhanced photosynthesis often increases total nonstructural carbohydrate (sugars and starches) concentrations within leaf tissues (Curtis & Wang, 1998; Long et al., 2004; Teng et al., 2006). Interestingly, recent studies indicate that carbohydrates function as hormone-like signals in many important physiological and developmental processes, such as the expression of genes involved in the control of photosynthetic downregulation at elevated CO2 (reviewed by Moore et al., 1999) and in the initiation of flowering (reviewed by Rolland et al., 2006).
Growth at elevated [CO2] also affects plant reproduction and development, both of which largely influence plant fitness. For example, in a meta-analysis, Jablonski et al. (2002) reported significant increases in the number of flowers (+19%), fruits (+18%), and seeds (+16%) for plants grown at elevated [CO2]. In addition, several studies have reported significant intraspecific variation in reproductive responses to elevated [CO2], increasing the potential for evolutionary changes at elevated [CO2] (Ward & Strain, 1997; Ward et al., 2000). In some cases, elevated [CO2] also alters developmental processes such as germination (Edwards et al., 2001; Hussain et al., 2001; Thurig et al., 2003; Mohan et al., 2004; Zavaleta, 2006), leaf development (Ainsworth et al., 2006), flowering time (reviewed here), and senescence (Rae et al., 2006). An understanding of plant developmental responses to elevated [CO2] is necessary for predictions of the long-term evolutionary outcomes of plants in a high-CO2 world. Unfortunately, relatively few studies have focused on these developmental responses relative to those examining the responses of plant gas exchange and growth (Ward & Kelly, 2004). Of the measurements examining developmental processes, the response of flowering time (defined here as the time to the first visible flower) has been commonly reported; however, until this point, a synthesis of this plant response to elevated [CO2] has not been put forward.
Changes in flowering time with elevated [CO2] have implications at several levels of biological organization, including the species, community and ecosystem levels. At the species level, changes in flowering time are likely to influence plant evolutionary processes, mainly because flowering time is an important life-history trait that has large effects on total reproductive output and potential fitness (Schemske, 1977; Waser, 1978; O’Neil, 1997). Although also important in long-lived species, this will be most important for annual species that have short generation times with the potential for rapid evolution (Ward et al., 2000). Typically for annual species, the onset of reproduction marks the end of the vegetative growth stage and begins the early stages of senescence (Simpson et al., 1999). As a result, elevated [CO2] may alter plant fitness both through changes in flowering time and through altered plant size at flowering, which influences the amount of resources available for reproduction (Ward et al., 2000). Furthermore, a species exhibiting delayed flowering at elevated [CO2] may not complete its life cycle before the end of the growing season in some climates (Ward & Kelly, 2004). In addition, Bazzaz (1990) hypothesized that plant fitness could be further constrained by changes in flowering time with elevated [CO2] through a decoupling of plant–pollinator developmental cycles. This would be especially relevant in future systems where high [CO2] leads to delayed flowering (even in the presence of other climate changes), while the concomitant increase in temperature results in accelerated development of insect pollinators (Bale et al., 2002). Although this phenomenon has yet to be observed experimentally with elevated [CO2], it is conceivable, as plant reproductive output is already constrained under current conditions by the lack of an adequate number of insect pollinators (Schemske & Lande, 1985; NRC, 2007).
At the community level, differential effects of elevated [CO2] on flowering time may lead to changes in community composition over long time scales by increasing competition between species (Tilman, 1982; Rathcke & Lacey, 1985). This scenario may also alter ecosystem productivity, because of the well established link between ecosystem productivity and biodiversity (Tilman et al., 1997). In support of this idea, Cleland et al. (2006) examined the developmental and productivity responses of naturally established grassland communities grown at elevated [CO2] at the Jasper Ridge Global Change Experiment in central California, USA. They reported accelerated flowering of forbs and delayed flowering of co-occurring grasses (both C3 and C4) when grown at elevated (approx. 680 ppm) relative to current (approx. 380 ppm) [CO2]. These elevated [CO2]-induced shifts in flowering time resulted in significant changes in the timing of peak net primary productivity as measured by the Normalized Difference Vegetation Index, probably through increased competition between forbs and grasses (Cleland et al., 2006). Because changes in flowering time with elevated [CO2] have the potential to have cascading effects from the individual through the ecosystem level, establishing a complete understanding of the responses of flowering time to growth at elevated [CO2], and the mechanisms involved in these responses, are of the utmost importance for accurately predicting and scaling the impact of elevated [CO2] on terrestrial ecosystems.
This review summarizes the current knowledge of flowering-time responses for plants grown at elevated [CO2]. Because of differences in the selection histories of crops and wild species, we evaluate their responses separately, but also conduct overall comparisons between the two types. Our review encompasses 60 studies that report measurements of flowering time among 90 species grown at elevated [CO2], and represents the most comprehensive synthesis of this response to date. We also discuss potential molecular and physiological mechanisms through which elevated [CO2] may be acting to influence the flowering time of plants. Finally, throughout the review, we offer suggestions where opportunities exist for future research.
It is well established that photoperiod, temperature and nutrient availability have large and often predictable effects on flowering time (Simpson et al., 1999). However, the effects of elevated [CO2] on flowering time are not as well understood, and vary widely among species. For instance, all possible responses have been observed both among species as well as within species, including accelerated, delayed and no change in flowering time in response to elevated [CO2] (Tables 1, 2). This large range of observations has occurred in highly controlled settings such as glasshouses (e.g. Ellis et al., 1995) and growth chambers (e.g. Ward & Strain, 1997), as well as in field settings that include open-top chambers (e.g. Curtis et al., 1994) and free-air carbon enrichment (FACE) sites (e.g. Cleland et al., 2006).
|Crop and cultivated species||Life cycle||[CO2] (ppm) treatments||Flowering time (d)||Reference|
|Avena sativa (oats)||Annual||590/743||No change||Sæbø & Mortensen (1996)|
|Capsicum annuum (pepper)||Annual||350/700||Accelerated||Peñuelas et al. (1995)|
|Chrysanthemum spp.||Perennial||330/900||No change||Mortensen (1986)|
|Cucumis sativus (cucumber)||Annual||350/1000||Accelerated||Peet 1986|
|Glycine max (soybean)||Annual||210/360/700||Delayed||Ellis et al. (1995)|
|G. max||Annual||350/700||No change||Nakamoto et al. (2004)|
|G. max||Annual||400/700||Accelerated (–2)||Heinemann et al. (2006)|
|G. max||Annual||350/700||Delayed||Rogers et al. (1984)|
|G. max||Annual||350/700||No change||Cooper & Brun (1967)|
|Gossypium hirsutum (cotton)||Annual||350/700||No change||Reddy et al. (1995)|
|Hordeum vulgare (barley)||Annual||400/700||Accelerated||Kleemola et al. (1994)|
|H. vulgare||Annual||590/743||No change||Sæbø & Mortensen (1996)|
|H. vulgare||Annual||350/700||Accelerated||Pukhal'skaya (1997)|
|Kalanchoe blossfeldiana||Perennial||330/1000||No change||Mortensen (1985)|
|Lycopersicon esculentum (tomato)||Annual||350/650||Accelerated||Micallef et al. (1995)|
|Oryza sativa (rice)||Annual||160/250/330/500/660/900||Accelerated||Baker et al. (1990)|
|O. sativa||Annual||350/700||Accelerated (–7)||Seneweera et al. (1994)|
|Petunia hybrida||Annual||350/1000||Accelerated (–15)||Reekie et al. (1997)|
|Pisum sativum (pea)||Annual||350/650||Accelerated||Musgrave et al. (1986)|
|Raphanus sativus (radish)||Annual||350/650||No change||Jablonski (1997)|
|Rosa hybrida||Perennial||330/900||Accelerated||Mortensen (1985)|
|Saintpaulia ionantha (African violet)||Perennial||330/900||Accelerated||Mortensen (1986)|
|Solanum tuberosum (Potato)||Annual||460/560/660||Accelerated||Miglietta et al. (1998)|
|Sorghum bicolor||Annual||210/360/700||Delayed||Ellis et al. (1995)|
|Triticum aestivum (wheat)||Annual||590/743||No change||Sæbø & Mortensen (1996)|
|Tropaeolum majus (nasturtium)||Annual||380/750||No change||Lake & Hughes (1999)|
|Vicia faba (bush bean)||Annual||350/700||Accelerated (–4)||Osborne et al. (1997)|
|Vigna unguiculata (blackeyed pea)||Annual||210/360/700||Accelerated||Ellis et al. (1995)|
|V. unguiculata||Annual||350/675/1000||Accelerated (–12)||Bhattacharya et al. (1985)|
|Begonia × hiemalis||Annual||330/990||Accelerated||Mortensen & Ulsaker (1985)|
|Zea mays (maize)||Annual||376/550||No change||Leakey et al. (2006)|
|Z. mays||Annual||350/550||Delayed||Hesketh & Hellmers (1973)|
|Wild species||Life cycle||[CO2] (ppm) treatments||Flowering time (d)||Reference|
|Abutilon theophrasti||Annual||300/600/900||No change||Garbutt & Bazzaz (1984)|
|A. theophrasti||Annual||350/500/700||No change||Garbutt et al. (1990)|
|A. theophrasti||Annual||350/700||No change||McConnaughay et al. (1993)|
|Achillea millefolium||Perennial||350/1000||Accelerated (–7)||Reekie et al. (1994)|
|Amaranthus retroflexus||Annual||350/500/700||Accelerated (–9)||Garbutt et al. (1990)|
|Ambrosia artemisiifolia||Annual||350/500/700||No change||Garbutt et al. (1990)|
|A. artemisiifolia||Annual||350/700||No change||Rogers et al. (2006)|
|Arabidopsis thaliana||Annual||360/1000||Delayed||Bae & Sicher (2004)|
|A. thaliana||Annual||350/700||No change||VanderKooij & DeKok (1996)|
|A. thaliana||Annual||350/700||Accelerated||Ward & Strain (1997)|
|A. thaliana||Annual||350/700||Delayed||Ward & Strain (1997)|
|Avena spp.||Perennial||380/680||Delayed (+6)||Cleland et al. (2006)|
|Betonica officinalis||Perennial||350/660||Accelerated (–8)||Rusterholz & Erhardt (1998)|
|Brassica napus||Annual||350/1000||Delayed||Frick et al. (1994)|
|Bromus diandrus||Perennial||380/680||Delayed (+3)||Cleland et al. (2006)|
|Bromus hordeaceus||Perennial||380/680||Delayed (+4)||Cleland et al. (2006)|
|Callistephus chinensis||Annual||350/1000||Accelerated (–5)||Reekie et al. (1994)|
|Calluna vulgaris||Perennial||350/450/550||Accelerated (–60)||Woodin et al. (1992)|
|Campanula isophylla||Perennial||350/1000||Accelerated (–14)||Reekie et al. (1994)|
|Campanula rotundifolia||Perennial||350/455||No change||Rämöet al. (2007)|
|Cardamine hirsuta||Annual||350/550||No change||Leishman et al. (1999)|
|Cassia faniculata||Annual||350/700||No change||Farnsworth & Bazzaz (1995)|
|Cassia nictitans||Annual||350/700||No change||Farnsworth & Bazzaz (1995)|
|Cassia obtusifolia||Annual||350/700||No change||Farnsworth & Bazzaz (1995)|
|Centaurea jacea||Perennial||350/660||No change||Rusterholz & Erhardt (1998)|
|C. jacea||Perennial||350/455||No change||Rämöet al. (2006)|
|Crepis vesicaria||Annual||380/680||Delayed (+4)||Cleland et al. (2006)|
|Datura stramonium||Annual||300/600/900||Accelerated (–2)||Garbutt & Bazzaz (1984)|
|Dendranthema grandiflora||Perennial||350/1000||Delayed (+1)||Reekie et al. (1994)|
|Dimorphotheca pluvalis||Annual||350/650||Delayed||Wand et al. (1996)|
|Dimorphotheca sinuate||Annual||360/700||No change||Musil et al. (1999)|
|Echinochloa crus-galli||Annual||350/675||Accelerated (–15)||Potvin & Strain (1985)|
|Eleusine indica||Annual||350/675||No change||Potvin & Strain (1985)|
|Epilobium angustifolium||Perennial||350/650||Accelerated (–2)||Erhardt et al. (2005)|
|Erodium botrys||Annual||380/680||Accelerated (–2)||Cleland et al. (2006)|
|Fragaria vesca||Perennial||350/455||No change||Rämöet al. (2007)|
|Gailardia pulchella||Annual||350/525/700||Accelerated (–6)||Reekie & Bazzaz (1991)|
|Geranium dissectum||Perennial||380/680||Accelerated (–2)||Cleland et al. (2006)|
|Gaura brachycarpa||Annual||350/525/700||Accelerated (–6)||Reekie & Bazzaz (1991)|
|Ipomoea hederacea||Annual||350/700||No change||Farnsworth & Bazzaz (1995)|
|Ipomoea lacunosa||Annual||350/700||No change||Farnsworth & Bazzaz (1995)|
|Ipomoea purpurea||Annual||350/700||No change||Farnsworth & Bazzaz (1995)|
|Kalanchoe blossfeldiana||Perennial||350/1000||Delayed (+4)||Reekie et al. (1994)|
|Lemna perpusilla||Perennial||300/600||Delayed||Posner (1971)|
|Lolium multiflorum||Perennial||380/680||Delayed (+6)||Cleland et al. (2006)|
|Lolium perenne||Perennial||350/600||No change||Wagner et al. (2001)|
|Lotus corniculata||Perennial||350/700||Accelerated (–7)||Carter et al. (1997)|
|L. corniculata||Perennial||350/660||No change||Rusterholz & Erhardt (1998)|
|Lupinus texensis||Annual||350/525/700||Delayed (+6)||Reekie & Bazzaz (1991)|
|Oenothera laciniata||Annual||350/525/700||Accelerated (–4)||Reekie & Bazzaz (1991)|
|Pharbitis nil||Annual||350/1000||Delayed (+5)||Reekie et al. (1994)|
|P. nil||Annual||30/100/1000/5000||Delayed||Hicklenton & Joliffe (1980)|
|Phlox drumondii||Annual||300/600/900||Accelerated||Garbutt & Bazzaz (1984)|
|Phytolacca americana||Perennial||370/740||No change||Wolfe-Bellin et al. (2006)|
|P. americana||Perennial||370/700||Accelerated (–3)||He et al. (2005)|
|P. americana||Perennial||370/700||Accelerated (–7)||He & Bazzaz (2003)|
|Poa annua||Annual||350/550||Accelerated (–4)||Leishman et al. (1999)|
|Polygonum hydropiper||Annual||350/700||No change||Farnsworth & Bazzaz (1995)|
|Polygonum lapathifolium||Annual||350/700||No change||Farnsworth & Bazzaz (1995)|
|Polygonum persicaria||Annual||350/700||No change||Farnsworth & Bazzaz (1995)|
|Ranunculus acris||Perennial||350/455||No change||Rämöet al. (2007)|
|Raphanus raphanistrum||Annual||350/670||No change||Case et al. (1998)|
|R. raphanistrum||Annual||338/685||No change||Curtis et al. (1994)|
|R. raphanistrum||Annual||350/650||No change||Jablonski (1997)|
|Scabiosa columbaria||Perennial||350/660||No change||Rusterholz & Erhardt (1998)|
|Senecio vulgaris||Annual||350/550||Accelerated (–4)||Leishman et al. (1999)|
|Setaria faberii||Annual||350/500/700||Delayed (+16)||Garbutt et al. (1990)|
|S. faberii||Annual||350/700||Delayed (+6)||McConnaughay et al. (1993)|
|Spergula arvensis||Annual||350/550||No change||Leishman et al. (1999)|
|Trachelium caeruleum||Perennial||350/1000||Accelerated (–12)||Reekie et al. (1994)|
|Trifolium medium||Perennial||350/455||No change||Rämöet al. (2007)|
|Trifolium pratense||Perennial||350/660||No change||Rusterholz & Erhardt (1998)|
|Trifolium repens||Perennial||350/600||Accelerated (–10)||Wagner et al. (2001)|
|Tropaeolum majus||Annual||380/750||No change||Lake & Hughes (1999)|
|Vicia cracca||Perennial||350/455||No change||Rämöet al. (2007)|
|Vicia sativa||Annual||380/680||Accelerated (–4)||Cleland et al. (2006)|
|Vulpia myuros||Annual||380/680||No change||Cleland et al. (2006)|
|Xanthium canadense||Annual||360/700||No change||Kinugasa et al. (2003)|
|Xanthium pensylvanicum||Annual||350/1000||Delayed (+2)||Reekie et al. (1994)|
Elevated [CO2] may also alter plant size at the time of flowering (Reekie & Bazzaz, 1991; Ward et al., 2000), and these responses have been shown to affect total reproductive output in annuals (Ward et al., 2000). In addition, flowering time changes may also influence resource availability for seed production during specific reproductive events in perennials (Stearns, 1992). Some species that exhibit accelerated flowering reach the minimum size required for flowering earlier because of enhanced growth rates at elevated [CO2] (He et al., 2005). However, other species exhibit delayed flowering at elevated [CO2], whereby they often reach the minimum size for flowering faster, but continue growing in a vegetative state until flowering at a later time and at a larger size (Reekie & Bazzaz, 1991; C. J. Springer & J. K. Ward, unpublished results). This type of altered flowering time represents a disruption in the overall developmental program, and mechanistically is more difficult to explain than accelerated flowering. In the future it will be important to distinguish accelerated from delayed flowering in CO2 studies, and to identify the primary mechanisms that account for both response types.
Elevated [CO2]-induced changes in flowering time have the potential to alter crop productivity and yield. Therefore understanding the flowering-time responses of crops should be of the utmost importance for crop-breeding programs aimed at maximizing yield in response to future environments. Fortunately, a substantial number of the studies reporting flowering-time responses at elevated [CO2] have been performed on either crop or cultivated species. An overwhelming majority of these studies have reported altered flowering time in response to elevated [CO2] (Table 1). In fact, among all studies reporting flowering time in crop and cultivated species, only seven of 23 species did not show evidence of altered flowering time during growth at elevated [CO2] (Table 1). Generally, most crop and cultivated species exhibiting differences in flowering timing at elevated [CO2] display accelerated flowering (Table 1). For example, rice (Oryza sativa) and barley (Hordeum vulgare) are some of the most economically important crop species that exhibit earlier flowering at elevated [CO2] (Table 1; Baker et al., 1990; Kleemola et al., 1994; Seneweera et al., 1994; Pukhal'skaya, 1997). On the other hand, crops such as sorghum (Sorghum bicolor) exhibit delayed flowering during growth at elevated [CO2] (Ellis et al., 1995).
Interestingly, two crop species that account for a substantial portion of the world's agricultural production, soybean (Glycine max) and maize (Zea mays), do not show consistent patterns in the response of flowering time at elevated [CO2]. In maize, an earlier study reported delayed flowering under elevated [CO2] (Hesketh & Hellmers, 1973), whereas a recent study reported no change in flowering time (Leakey et al., 2006). This discrepancy is probably a product of the growth conditions in each of the experiments: Hesketh & Hellmers (1973) performed their study in environmentally controlled growth chambers, and the study of Leakey et al. (2006) was performed using FACE technology under field conditions. In addition, the cultivars used in these studies may have influenced the observed differences in flowering time.
More difficult to explain is the variation in flowering-time responses to elevated [CO2] observed in soybean. Of the five studies reporting flowering-time responses during growth at elevated [CO2], two reported delayed flowering (Rogers et al., 1984; Ellis et al., 1995); one reported accelerated flowering, although this acceleration was significant at only one of three day : night growth temperatures (25 : 20°C) (Heinemann et al., 2006); and the remaining studies reported no changes in flowering time with elevated [CO2] (Cooper & Brun, 1967; Nakamoto et al., 2004). Rogers et al. (1984) hypothesized that the growth habits, namely indeterminant vs determinant, of the cultivars used in these studies may account for the differential responses of flowering time to elevated [CO2]. For example, Cooper & Brun (1967) reported no alterations in flowering time with elevated [CO2] in an indeterminant cultivar of soybean, whereas Rogers et al. (1984) used a determinant variety of soybean that exhibited delayed flowering with elevated [CO2]. This discrepancy suggests that the determinate cultivar may have had reduced demand (lower sink strength) for photosynthate during growth at elevated [CO2], a factor that commonly alters plant responses to elevated [CO2] (Tissue et al., 1999). However, in subsequent studies, indeterminant cultivars also yielded varying results with respect to the responses of flowering time to elevated [CO2] (Ellis et al., 1995; Nakamoto et al., 2004). These results illustrate the potential for altered flowering time in some of the most important crops in response to future [CO2], and also suggest that predicting these responses in advance may be highly challenging.
An additional observation that can be made from the above studies is that plants utilizing both the C3 (e.g. soybean) and C4 (e.g. maize) photosynthetic pathways show altered flowering time with elevated [CO2]. This result is somewhat surprising, as C4 plants commonly show less pronounced physiological responses (photosynthesis and biomass accumulation) to growth at elevated [CO2] than C3 plants (Dippery et al., 1995; Wand et al., 1999). Taken together, these findings suggest that even small changes in physiological functioning of plants grown at elevated [CO2], such as those commonly observed in C4 species (Wand et al., 1999), are sufficient to alter flowering time, although this area is in critical need of additional research.
The transition from vegetative to reproductive growth is one of the most important developmental milestones in crops, particularly as the timing of this transition can have major impacts on final yield. Unfortunately, the few studies that have examined crop flowering-time responses to elevated [CO2] are by no means exhaustive, and therefore an accurate prediction of crop responses in the future is not possible at this time. Changes in flowering time in response to elevated [CO2] will have an economic impact on agricultural producers if changes in flowering time and yield occur simultaneously with rising [CO2]. Therefore more studies are needed that examine the relationships between elevated [CO2]-induced changes in flowering time and final yield, and these would be most informative for establishing future predictions if conducted in field settings (such as Miglietta et al., 1998; Leakey et al., 2006).
The overall pattern of flowering-time responses of wild species grown at elevated [CO2] varies from the pattern observed in crops and cultivated species. Flowering-time responses of wild species grown at elevated [CO2] are much more evenly distributed, in that a similar number of studies report accelerated, delayed, or no change in flowering time (Table 2), whereas crops primarily showed accelerated flowering (approx. 80% exhibited accelerated flowering). One possible explanation for this discrepancy is that many of the crop species presented are annuals, whereas the wild species include both annuals and perennials (Tables 1, 2). However, the flowering-time responses of wild species to growth at elevated [CO2] show a nearly equal proportion of annuals and perennials exhibiting accelerated, delayed, and no changes in flowering time (Table 2). Interestingly, the more unidirectional response for flowering time in crops relative to wild species is probably the consequence of artificial selection in crop species vs natural selection in wild species. Crop species are often selected for earlier flowering in order to maximize yield in the shortest time possible, thus decreasing the likelihood of catastrophic losses from drought or frost. However, the variation in the responses of flowering time of wild species grown at elevated [CO2] probably reflects various developmental strategies that maximize fitness across a range of environmental conditions. The adaptation of earlier flowering in many species is related to a stress-avoidance strategy that enables completion of the life cycle before a drought or cold period, much like the case of artificial selection for hastened development in crop species (Roux et al., 2006). Alternatively, delayed flowering leads to an extension of vegetative growth that maximizes available resources for reproduction, which serves to enhance fitness during years when the growing season is extended, or in regions where the growing season is more continuous (Roux et al., 2006).
The magnitude of the flowering-time response of wild species also varies considerably from one species to the next. For example, Calluna vulgaris exhibited the largest response, where plants flowered 60 d earlier at even modest increases in [CO2] (current + 100 ppm CO2) (Woodin et al., 1992). In contrast, the longest observed delay in flowering time was found in Setaria faberii, where plants flowered 16 d later at elevated [CO2] (700 ppm; Garbutt et al., 1990). In many cases, the responses of flowering time to elevated CO2 in wild species show similar patterns when compared across multiple studies performed on the same species, unlike the example of soybean presented earlier. For instance, multiple studies have consistently found no change in the response of flowering time at elevated [CO2] for Raphanus raphanistrum (Curtis et al., 1994; Jablonski, 1997; Case et al., 1998), Abutilon theophrasti (Garbutt & Bazzaz, 1984; Garbutt et al., 1990; McConnaughay et al., 1993), Ambrosia artemisiifolia (Garbutt et al., 1990; Rogers et al., 2006), and Centaurea jacea (Rusterholz & Erhardt, 1998; Rämöet al., 2006). Also, the onset of flowering has been consistently delayed at elevated [CO2] in S. faberii (Garbutt et al., 1990; McConnaughay et al., 1993) and Pharbitis nil (Hicklenton & Joliffe, 1980; Reekie et al., 1994). In some cases, however, species do show variation in the response of flowering time across multiple studies. In the case of Lotus corniculata, one study found a significant acceleration of flowering (Carter et al., 1997), while a different study reported no change in flowering time at elevated [CO2] (Rusterholz & Erhardt, 1998). Additionally, of the three studies examining the flowering-time responses of Phytolacca americana to elevated [CO2], two reported significantly earlier flowering at elevated [CO2] (He & Bazzaz, 2003; He et al., 2005), whereas the third study found no difference in flowering time (Wolfe-Bellin et al., 2006). These discrepancies could be related to the different growth conditions that were used between experiments, such as light, water or nutrient levels. In addition, the use of different genotypes across the experiments may also be responsible for the variation in observed flowering-time responses (see Fig. 1 for an example of this variation in Arabidopsis thaliana).
The examples of studies performed within a genus also show a lack of consistent flowering-time response to elevated [CO2] (Table 2). Specifically, only Bromus (Cleland et al., 2006), Cassia (Farnsworth & Bazzaz, 1995), Ipomoea (Farnsworth & Bazzaz, 1995) and Polygonum (Farnsworth & Bazzaz, 1995) exhibited no changes in flowering time at elevated [CO2] in multiple studies examining different species within these genera. Genera exhibiting interspecific variation in the degree of flowering-time response with elevated [CO2] include Campanula (Reekie et al., 1994; Rämöet al., 2007), Dimorphotheca (Wand et al., 1996; Musil et al., 1999), Lolium (Wagner et al., 2001; Cleland et al., 2006), Trifolium (Rusterholz & Erhardt, 1998; Wagner et al., 2001; Rämöet al., 2007), Vicia (Cleland et al., 2006; Rämöet al., 2007) and Xanthium (Reekie et al., 1994; Kinugasa et al., 2003). Such a range of responses within a genus may reflect localized adaptations between species that interact with elevated [CO2] to alter flowering time. The potential for the interaction of localized adaptations with growth at elevated [CO2] stresses the need for studies examining intraspecific variation in the responses of flowering time to elevated [CO2].
A very limited number of studies have examined intraspecific variation in the response of flowering time to elevated [CO2]. These studies have found that some species exhibit significant genetic variation in the response of flowering time at elevated [CO2], while other species do not (Garbutt & Bazzaz, 1984; Curtis et al., 1994; Case et al., 1998). For instance, elevated [CO2] accelerated flowering in Phlox drumondii, but this effect did not depend on the population type (Garbutt et al., 1984). Also, two studies examining multiple genotypes of R. raphanistrum found no changes in flowering time for elevated [CO2]-grown plants. Alternatively, we found significant genetic variation in the response of flowering time among genotypes of A. thaliana grown over a single generation at current (380 ppm) and elevated (700 ppm) CO2 (Fig. 1). Despite only testing 10 genotypes in this study, all possible flowering-time responses to elevated [CO2], including delayed, accelerated and unaltered flowering times, were observed between 380 and 700 ppm CO2. These genotypes originated from widely distributed geographical regions representing large amounts of variation in environmental parameters such as temperature, water availability and photoperiod. Thus these genotypes were exposed to differing selection pressures in their respective provenances that probably influenced their responses to CO2. This further suggests that life-history traits and localized adaptations influence the effects of elevated [CO2] on flowering time. In a different study, Ward et al. (2000) examined the responses of A. thaliana genotypes selected for high fitness (seed number) at elevated [CO2] over five generations. Interestingly, the response of flowering time was far more important in conferring increased fitness in elevated [CO2]-evolved genotypes than any other trait, including biomass accumulation. This finding further illustrates the importance of a complete understanding of the responses of flowering time at elevated [CO2], especially for predicting the future evolutionary trajectories of wild plant species.
Because atmospheric [CO2] is rising along with changes in other features of climate, such as water availability and temperature, understanding the interactive effects of elevated [CO2] with other climate change factors is critical for both crop and wild species. Surprisingly, a majority of multifactor studies that measured flowering time report no interaction between elevated [CO2] and other environmental factors, such as temperature in Gossypium hirsutum (Reddy et al., 1995) and H. vulgare (Pukhal'skaya, 1997); nutrient availability in Raphanus sativus, R. raphanistrum (Jablonski, 1997), O. sativa (Seneweera et al., 1994), H. vulgare (Kleemola et al., 1994) and Dimorphotheca sinuate (Musil et al., 1999); light in Cardamine hirsuta (Leishman et al., 1999) and G. max (Nakamoto et al., 2004); and ozone in Ranunculus acris, Trifolium medium, Vicia cracca, Fragaria vesca, C. jacea and Campanula rotundifolia (Rämöet al., 2007). However a limited number of elevated [CO2] studies do show significant interactive effects with other environmental factors on flowering time, and these are worth careful consideration because of the implications of these results. In one example, when considered independently, elevated [CO2] decreased the time of flowering by 5 d in L. corniculata, while growth at high temperature decreased the time of flowering by 7 d (Carter et al., 1997). However, when elevated [CO2] and high temperature were combined, the result was an acceleration of flowering by 16 d in L. corniculata. Such a response indicates that, for some species, elevated [CO2] may accentuate the effects of rising temperatures on development rate. In the same experiment, water availability also modulated the responses of flowering time of L. corniculata plants grown at elevated [CO2]. Interestingly, plants grown under saturated conditions showed no changes in flowering time in response to elevated [CO2], but exhibited accelerated flowering when grown at elevated [CO2] with drought conditions (Carter et al., 1997). It is also important to note that, although global warming has received the most attention for its influence on flowering time, increasing [CO2] may actually override the effects of warming in some cases. For example, Cleland et al. (2006) recently showed that several grass species grown at elevated [CO2] (680 ppm) delayed flowering by 2–7 d, depending on the species. On the other hand, the high-temperature treatment (+1.5°C) at current [CO2] accelerated flowering of grasses by 2–5 d, when combined, elevated [CO2] acted in an additive fashion to completely eliminate the effects of warming on earlier flowering. The results of these studies strongly suggest that, in addition to warming, the influence of other global change factors such as elevated [CO2] on flowering time must be considered, and the interactions of multiple factors may produce unexpected results with regard to developmental processes.
The ability to predict accurately future impacts of changes in flowering time on higher scales of organization depends largely on the degree to which responses can be generalized across species and environmental conditions. Currently, the substantial variation observed in flowering-time responses to elevated [CO2], both among and within species, makes generalizing these responses difficult. In order to address this issue, it will be important to understand the primary physiological and molecular mechanisms that influence developmental processes in response to elevated [CO2]. It is likely that once these mechanisms are understood, probably through using model systems (A. thaliana), they can be expanded to other species, as the mechanisms controlling flowering time are highly (although not entirely) conserved across a broad range of species (Simpson & Dean, 2002).
Understanding the primary mechanisms controlling flowering-time responses at elevated [CO2] has other potential benefits as well. For example, future work on these primary mechanisms may provide new insights into our understanding of how environmental and endogenous cues interface with already well defined floral developmental pathways. Also, incorporation of such mechanisms into crop-breeding programs will be beneficial for maximizing crop productivity in the face of future increases in [CO2], and may contribute to feeding an ever-increasing global population. Finally, many evolutionary models depend on knowledge of the molecular and physiological mechanisms that influence traits acted on by natural selection, such as flowering time, in order to predict selection responses (Ward & Kelly, 2004). Therefore knowledge of the mechanisms controlling the response of flowering time to elevated [CO2] will probably bolster modeled projections of future plant evolution, while also increasing the empirical predictability of future plant responses to elevated [CO2].
A small volume of excellent work has been performed with the primary objective of uncovering the underlying mechanisms that control elevated [CO2]-induced changes in flowering time. For example, Reekie & Bazzaz (1991) initially hypothesized that observed changes in development associated with elevated [CO2] were primarily a function of changes in plant growth rate at elevated [CO2]. More specifically, the authors hypothesized that as elevated CO2 increased growth rates, plants would reach the minimum size necessary for flowering faster. To test this idea, they grew Gaura brachycarpa, Gailardia pulchella, Oenothera laciniata and Lupinus texensis at 350, 550 and 700 ppm CO2 in three different pot sizes, and included treatments where plants were grown in competition (several individuals per pot) and individually without competition. Subsequently, elevated [CO2] resulted in accelerated, delayed and unaltered flowering times, and the responses were affected by both pot size and competitive interactions. However, enhanced relative growth rates at elevated [CO2] did not result in accelerated flowering, and in some cases produced delayed flowering (Reekie & Bazzaz, 1991). It is important to note, however, that He et al. (2004) did find that enhanced relative growth rates resulted in accelerated flowering in P. americana grown at elevated [CO2] (700 ppm).
Others have proposed that photoperiod requirements may play some role in influencing the effects of elevated [CO2] on flowering time. For example, Reekie et al. (1994) examined the interaction of species and the effects of elevated [CO2] on the flowering time of four short-day species and four long-day species. Interestingly, all four short-day species exhibited delayed flowering between 350 and 1000 ppm CO2, whereas the four long-day species showed accelerated flowering between the two [CO2] treatments. These results supported the authors’ hypothesis that the response of flowering time to elevated [CO2] is associated with the photoperiodic requirements of species, suggesting that floral signaling pathways that are influenced by photoperiod may interact with elevated [CO2]. However, as Reekie et al. (1994) noted, other studies have shown variation in the response of flowering time with respect to the photoperiodic requirement (either long-day or short-day) of plants at elevated [CO2], particularly in short-day species (such as Mortensen, 1986, 987). To explain this variation, Reekie et al. (1994) concluded that differences in the length of inductive photoperiods used during CO2 enrichment among these various experiments might explain the variation in response. The authors further stressed that to establish correctly the possible link between photoperiodic responses and growth at elevated [CO2], all plant types should be grown under identical, inductive photoperiods (Reekie et al., 1994). To test this hypothesis further, Ellis et al. (1995) examined the rate of development of three short-day species (S. bicolor, G. max and Vigna unguiculata) in response to growth at elevated [CO2] under identical 11 h d−1 inductive photoperiods. Increased [CO2] accelerated the flowering time of V. unguiculata; however, flowering in both S. bicolor and G. max was delayed at elevated [CO2]. Ellis et al. (1995) concluded, similarly to Reekie et al. (1994), that increasing [CO2] did not affect flowering time through increases in growth rate, but rather through alterations in plant size at flowering. Furthermore, these results did not support the hypothesis that plant developmental responses at elevated [CO2] are consistently related to the photoperiodic requirements of the species in question, mainly because Ellis et al. (1995) found both accelerated and delayed flowering in response to elevated [CO2] in three short-day species under identical inductive photoperiods.
To our knowledge, these studies represent the extent of the direct tests of the mechanisms that lead to altered flowering time and plant size at flowering in elevated [CO2]-grown plants. Although these findings provide a valuable start for elucidating the mechanisms of elevated [CO2]-induced alterations in flowering time, much more work is needed in this area. Especially valuable for future consideration are studies examining mechanisms related to altered size at flowering, and studies examining the mechanisms behind delayed flowering at elevated [CO2], because such responses are probably the result of a significant disruption in the developmental program of plants that is produced by elevated [CO2].
Many studies have implicated carbohydrates (sugars and starches) as playing a role in the control of flowering time, as carbohydrates can function as signaling molecules (for a detailed review of carbohydrate sensing and signaling in plants see Rolland et al., 2006). Because C3 plants grown at elevated [CO2] commonly accumulate excess carbohydrates in leaves (Curtis & Wang, 1998; Long et al., 2004), this may be one possible mechanism through which elevated [CO2] may be influencing flower timing. Past studies examining plants with altered carbon metabolism, manifested either through growth conditions (e.g. high light or excess sugars in the growth medium) or through mutations, may be particularly useful in determining the mechanism(s) involved in altered flowering time at elevated [CO2], as they share the similar characteristic of producing excess carbohydrates in leaves. For example, several mutants of A. thaliana such as cam1, pgm (AT5G51820), adg1 (AT5G48300) and sex1 (AT1G10760), which exhibit altered starch metabolism leading to increased tissue sugar concentrations, all exhibit late-flowering phenotypes (Caspar et al., 1985, 1991; Lin et al., 1988; Eimert et al., 1995). Other recent evidence also strengthens the link between carbohydrates and the control of flowering time, whereby A. thaliana plants with a mutation in the trehalose-6-phosphate synthase gene (AT1G78580), a gene closely associated with both sugar signaling and starch metabolism, failed to flower (van Dijken et al., 2004).
Other studies have also indicated that differences in exogenous sugars in the growth medium can influence flower timing. In a highly interesting study, Zhou et al. (1998) observed delayed flowering in A. thaliana grown in the dark on medium containing 6% sucrose relative to medium containing 2% sucrose, whereas a glucose-insensitive mutant (gin1; AT1G52340) did not exhibit such sensitivity. In addition, Ohto et al. (2001) observed an 8-d delay in flowering of A. thaliana grown on growth medium containing 5% compared with 1% sucrose. This response coincided with a significant increase in the number of adult rosette leaves present at the time of flowering, and an increase in overall plant size at flowering. Furthermore, the length of time that plants received more sucrose increased the severity of the delay, suggesting a threshold for the response of flowering to additional sugar (Ohto et al., 2001). Interestingly, Ohto et al. (2001) also reported delayed flowering of A. thaliana grown with higher levels of exogenous sucrose in the growth medium that involved delays in the up-regulation of a key meristem identity gene LEAFY (LFY, AT5G61850). This delayed upregulation of LFY indicates that carbohydrates affect the expression of genes involved in the floral development pathway, either directly or indirectly (Ohto et al., 2001), and that elevated [CO2] may also influence the expression of floral timing and development genes via alterations in carbohydrate status. Further evidence supporting the role of carbohydrates in controlling flowering time through altered gene expression comes from a recent study by Wilson et al. (2005). The authors characterized the molecular phenotypes of A. thaliana mutants for flowering-time genes by generating global gene-expression profiles with whole-genome microarray technology. This study concluded that genes with functions associated with metabolism exhibited the largest changes in expression across all the flowering-time mutants, indicating an intimate link between flowering time and carbon metabolism (Wilson et al., 2005).
Although the precise mechanisms of carbohydrate controls of flowering time have yet to be fully elucidated, several other plant processes are regulated through carbohydrate sensing and signaling, such as germination, carbon and nitrogen metabolism, hormonal signaling, stress responses, and senescence (Rolland et al., 2006). Additionally, the association between increased carbohydrates resulting from plant growth at elevated [CO2] and feedbacks from these excess carbohydrates through signaling processes to restrict the expression of photosynthetic genes has already been clearly established (commonly known as CO2 acclimation or photosynthetic downregulation; Moore et al., 1999). Given the links between carbon metabolism and flowering time, it is possible that excess sugars produced at elevated [CO2] may also serve to signal the onset of flowering. With regard to photosynthetic downregulation, Moore et al. (1999) noted that the intra- and interspecific variation in photosynthetic downregulation might be caused by a threshold sugar concentration, whereby species and genotypes exhibit differential sensitivity to increased foliar sugar levels. Therefore it is possible that a similar threshold effect of sugar sensitivity may explain the intra- and interspecific variation that is observed in elevated [CO2]-induced alterations in flowering time. In addition, it has been shown in A. thaliana that meristem-specific overexpression of cell wall invertases, an important suite of enzymes involved in elevated [CO2]-induced downregulation of photosynthesis, leads to advancement of flowering time; however, overexpression of cytosolic invertases leads to delayed flowering (Heyer et al., 2004). Taken together, these findings indicate that similar mechanisms responsible for CO2 acclimation of photosynthesis may also be controlling altered flowering time at elevated [CO2].
Unfortunately, the link between excess foliar sugars and altered flowering time of elevated [CO2]-grown plants has not been tested directly. However, the results of previous elevated-[CO2] studies do support such a hypothesis. In the early 1970s, Posner (1971) observed a link between increased foliar sugars and delayed flowering in Lemna perpusilla by showing that growth at elevated [CO2] or with additions of sucrose to the growth medium led to similar delays in flowering time. Interestingly, flowering was further delayed when plants were grown with a combination of elevated [CO2] and medium containing additional sucrose. As mentioned above, Rogers et al. (1984) observed an elevated [CO2]-induced delayed flowering in a determinate variety of soybean that resulted in a slower transition from the adult vegetative stage to the reproductive stage. However, in an earlier study, elevated [CO2] had no effect on the timing of flowering in an indeterminate variety of soybean (Cooper & Brun, 1967). This discrepancy suggests that the determinate variety may have had reduced demand (lower sink strength) for photosynthate during growth at elevated [CO2], a phenomenon that commonly results in excess sugar accumulation in leaves (Tissue & Wright, 1995). Furthermore, the commonly studied genotype of A. thaliana Columbia exhibited delayed flowering when grown at elevated [CO2] (1000 ppm). This delay was accompanied by a 41% increase in foliar sucrose concentration and a 105% increase in foliar starch concentration (Bae & Sicher, 2004).
Understanding the interactions between carbohydrate-regulated gene expression and their effects on flowering time should be given high priority in future studies, especially under realistic levels of increased carbohydrates that are relevant to the effects of rising CO2. Nonetheless, this represents only one potential mechanism for altered flowering time at elevated [CO2], and therefore investigations examining other possible mechanisms must also be given full consideration. In addition, most of the progress made in determining the general mechanisms responsible for the control of flowering time has been made using the annual A. thaliana. Although the mechanisms controlling flowering time in A. thaliana are highly conserved across a broad range of plant species (Simpson & Dean, 2002; Tan & Swain, 2006), direct efforts should also be made to understand how elevated [CO2] may alter the flowering time of perennials and the mechanisms accounting for these response, as these may potentially vary from annuals (Simpson & Dean, 2002; Tan & Swain, 2006).
The studies reviewed here clearly show that future increases in atmospheric [CO2] will have major effects on the flowering time of both wild and crop species. It is also clear that such responses may alter the competitive interactions of species and may influence net primary productivity at the ecosystem level. This review also points out that flowering-time responses at elevated [CO2] may be highly variable both among (e.g. wild and crop species) and within species. Although the studies included in this review have provided valuable insights, at this time it is not possible to account for the wide variation in flowering-time responses because knowledge of the underlying physiological and molecular mechanisms is incomplete. In addition, the majority of available studies focusing on the effects of elevated [CO2] have used highly controlled growth conditions (e.g. growth chambers, glasshouses). Such work is of great value, especially for elucidating the mechanisms responsible for elevated [CO2]-induced changes in flowering time. However, more work is also needed that examines the developmental responses of plants grown in natural settings in order to better determine the implications of altered flowering time on ecosystem processes and agricultural productivity. Furthermore, future studies examining the interactive effects of elevated [CO2] with other environmental factors known to influence flowering time (light, temperature and nutrients) will be particularly useful in predicting the long-term responses of plants to elevated [CO2]. Finally, past studies have provided striking evidence that carbon metabolism exerts at least partial control on flowering time. By utilizing this information, we are now in an excellent position to begin detailed examinations of the primary mechanisms through which elevated [CO2] alters flowering time while also furthering our fundamental understanding of the basic biological controls of flowering time.
We would like to thank Dr Jesse Nippert, and three anonymous referees whose insight greatly improved this manuscript. We would also like to thank Rebecca Orozco for her help with the literature survey. Funds from the National Science Foundation (0517668) and the US Department of Agriculture (2003-35100-13576) supported C.J.S. and J.K.W. during preparation of this manuscript.