With global change, atmospheric carbon dioxide (CO2) concentration is predicted to rise from today's value of c. 370–550 ppm by 2050 and could reach between 730 and 1010 ppm by 2100 (Solomon et al. Reference Solomon, Qin, Manning, Chen, Marquis, Averyt, Tignor, Miller, Solomon, Qin, Manning, Chen, Marquis, Averyt, Tignor and Miller2007). This, combined with other atmospheric changes, is projected to increase global mean temperatures by 1·4–5·8 °C (Houghton et al. Reference Houghton, Ding, Griggs, Noguer, Van Der Linden, Dai, Maskell and Johnson2001). Jaggard et al. (Reference Jaggard, Qi and Ober2010) concluded that CO2 enrichment was likely to allow yield increases of c. 13% in most C3 crops, but yields of C4 crops are not expected to change. However, increasing temperatures may negate these increases in C3 crops, particularly if they occur during reproductive growth (Allen & Boote Reference Allen, Boote, Reddy and Hodges2000; Wheeler et al. Reference Wheeler, Craufurd, Ellis, Porter and Prasad2000). Gornall et al. (Reference Gornall, Betts, Burke, Clark, Camp, Willett and Wiltshire2010) noted that extreme weather events are more likely to occur in the changed climate of the future, and predicted that over much of the world's crop land, maximum daily temperature highs may be increased by around 3 °C by 2050.
A major challenge ahead for those involved in the seed industry, therefore, is to provide cultivars that can maximize future crop production in a changing climate (Ainsworth et al. Reference Ainsworth, Rogers and Leakey2008a; Bruins Reference Bruins2009; Ceccarelli et al. Reference Ceccarelli, Grando, Maatougui, Michael, Slash, Haghparast, Rahmanian, Taheri, Al-Yassin, Benbelkacem, Labdi, Mimoun and Nachit2010). Ainsworth et al. (Reference Ainsworth, Beier, Calfapietra, Ceulemans, Durand-Tardif, Farquhar, Godbold, Hendrey, Hickler, Kaduk, Karnosky, Kimball, Körner, Koornneef, Lafarge, Leakey, Lewin, Long, Manderscheid, McNeil, Mies, Miglietta, Morgan, Nagy, Norby, Norton, Percy, Rogers, Soussana, Stitt, Weigel and White2008b) considered that this will be possible within a decade.
Successful crop production in any environment depends initially on the quality of the seed being sown. The term ‘seed quality’ is used in practice to describe the overall value of a seed lot for its intended purpose (Hampton Reference Hampton2002), and includes the components of species and cultivar purity, seed mass (size), physical purity, germination, vigour, moisture content and seed health. The present review examines the effects of increased CO2 and increased temperature on three of these seed quality components, seed mass, germination and vigour.
Within the seed industry, seed size is commonly denominated by the mean seed weight, often expressed as ‘thousand seed weight’, the weight of 1000 seeds of the seed lot. However, seed size refers to volume, while seed weight and seed mass refer to density, which are different traits (Castro et al. Reference Castro, Hodar, Gomez and Basra2006). Seed mass in crop cultivars is considered the least variable of the seed yield components because of plant breeding for increased seed uniformity (Almekinders & Louwaars Reference Almekinders and Louwaars1999) and the removal of small seeds during the seed cleaning processes. Factors affecting seed mass, including genetic factors, water availability and nutrient availability were reviewed by Castro et al. (Reference Castro, Hodar, Gomez and Basra2006).
Increased atmospheric CO2 concentrations might be expected to increase seed mass because of increased plant assimilate availability (Jablonski et al. Reference Jablonski, Wang and Curtis2002), but the reported effects of elevated CO2 are highly variable among species (Miyagi et al. Reference Miyagi, Kinugasa, Hikosaka and Hirose2007; Hikosaka et al. Reference Hikosaka, Kinugasa, Oikawa, Onoda and Hirose2011). Different studies have reported seed mass to increase (Musgrave et al. Reference Musgrave, Strain and Siedow1986; Baker et al. Reference Baker, Allen, Boote, Jones and Jones1989; Dijkstra et al. Reference Dijkstra, Schapendonk, Groenwold, Jansen and van de Geijn1999; Steinger et al. Reference Steinger, Gall and Schmid2000; Quaderi & Reid Reference Quaderi and Reid2005), show no change (Edwards et al. Reference Edwards, Clark and Newton2001; Prasad et al. Reference Prasad, Boote, Allen and Thomas2002) and decrease (Huxman et al. Reference Huxman, Hamerlynck, Jordan, Salsman and Smith1998; Smith et al. Reference Smith, Huxman, Zitzer, Charlet, Housman, Coleman, Fenstermaker, Seemann and Nowak2000; Wagner et al. Reference Wagner, Luscher, Hillebrand, Kobald, Spitaler and Larcher2001) in response to elevated CO2. Jablonski et al. (Reference Jablonski, Wang and Curtis2002) conducted a meta-analysis of 184 CO2 enrichment studies from 79 species and found a mean 4% increase in seed mass, with the response being greater in legumes (+8%) than non-legumes (+3%), and absent in C4 plants. Considerable variation in seed mass in response to elevated CO2 was also reported within species. Hikosaka et al. (Reference Hikosaka, Kinugasa, Oikawa, Onoda and Hirose2011) reported the enhancement ratio of seed mass per plant (seed mass in elevated CO2/seed mass in ambient CO2) ranged from 0·75 to 4·45 in rice (Oryza sativa L.), from 0·93 to 1·87 in soybean (Glycine max (L.) Merrill), and from 0·88 to 2·07 in wheat (Triticum aestivum L.).
Jablonski et al. (Reference Jablonski, Wang and Curtis2002) found a 14% reduction in seed nitrogen (N) in response to elevated CO2 averaged across all 79 species in their analysis, although there was significant variation; seed N was not reduced in legumes, but was reduced in non-legumes. Hikosaka et al. (Reference Hikosaka, Kinugasa, Oikawa, Onoda and Hirose2011) suggested that seed mass could only increase when N became more available at elevated CO2 concentrations. Legumes may use increased carbon (C) gain under elevated CO2 for increased nitrogen fixation (Allen & Boote Reference Allen, Boote, Reddy and Hodges2000), and can therefore increase seed mass without decreasing seed N. In non-legumes, seed mass increases may result in a decrease in seed N concentration. In some species, this decreased seed N may be at the expense of seed quality (Fenner Reference Fenner1991; Andalo et al. Reference Andalo, Godelle, Lefranc, Mousseau and Till-Bottraud1996).
Increasing temperature can negate the response to elevated CO2 (Prasad et al. Reference Prasad, Boote, Allen and Thomas2002) and may reduce seed mass (Spears et al. Reference Spears, Tekrony and Egli1997) because of the resulting acceleration in seed growth rate (dry matter accumulation) and reduction in the duration of seed filling (Weigand & Cueller Reference Weigand and Cueller1981; Young et al. Reference Young, Wilen and Bonham-Smith2004). However, a reduction in the rate of seed dry matter accumulation can also occur (Gibson & Paulsen Reference Gibson and Paulsen1999) and seed mass has also been reported not to change, or sometimes increase, in response to temperature increase (Peltonen-Sainio et al. Reference Peltonen-Sainio, Jauhiainen and Hakala2011). A reduced seed mass for a seed lot does not necessarily mean a loss in other seed quality attributes. Many studies have shown no relationship between seed mass and germination (Castro et al. Reference Castro, Hodar, Gomez and Basra2006) or seed mass and seed vigour (Powell Reference Powell1988).
For high-quality seed lots, germination (defined as the process that begins with imbibition and which is completed by the production of a normal seedling; ISTA 2011) is desired by the seed industry to be as close to 100% as possible. The germination of a seed lot can be negatively affected by the conditions the seeds are exposed to during harvesting, drying, cleaning and storage, but can also be reduced by unfavourable environmental conditions in the field during seed growth and development (Dornbos Reference Dornbos and Basra1995), particularly temperature, rainfall and relative humidity (Egli et al. Reference Egli, Te Krony, Heitholt and Rupe2005).
Seed germination in response to elevated CO2 has been reported to decrease (Farnsworth & Bazazz Reference Farnsworth and Bazazz1995; Andalo et al. Reference Andalo, Godelle, Lefranc, Mousseau and Till-Bottraud1996; Quaderi & Reid Reference Quaderi and Reid2005), show no change (Huxman et al. Reference Huxman, Hamerlynck, Jordan, Salsman and Smith1998; Steinger et al. Reference Steinger, Gall and Schmid2000; Thomas et al. Reference Thomas, Prasad, Boote and Allen2009; Way et al. Reference Way, Ladeau, Mccarthy, Clark, Oren, Finzi and Jackson2010) or increase (Wulf & Alexander Reference Wulf and Alexander1985; Ziska & Bunce Reference Ziska and Bunce1993; Edwards et al. Reference Edwards, Clark and Newton2001). The responses vary among species (Ziska & Bunce Reference Ziska and Bunce1993) and genotypic variation has also been reported (Andalo et al. Reference Andalo, Godelle, Lefranc, Mousseau and Till-Bottraud1996).
Elevated CO2 has been shown to increase the C/N ratio in seeds (Huxman et al. Reference Huxman, Hamerlynck, Jordan, Salsman and Smith1998; Steinger et al. Reference Steinger, Gall and Schmid2000; He et al. Reference He, Flynn, Wolfe-Bellin, Fang and Bazzaz2005) and in non-legumes, seed N reduction can occur when seed mass is increased by elevated CO2 (see previous section). High seed N is an advantage for germination rate (Hara & Toriyama Reference Hara and Toriyama1998), but not germination per se. However, a change in C/N ratio can lead to a decrease in seed protein content, resulting in a reduction in the ability of the seed to supply the amino acids required for the de novo protein synthesis necessary for embryo growth in the germinating seed. This could reduce seed viability (Andalo et al. Reference Andalo, Godelle, Lefranc, Mousseau and Till-Bottraud1996).
Elevated CO2 also increases ethylene production (Esashi et al. Reference Esashi, Ooshima, Michihara, Kurota and Satoh1986) and Ziska & Bunce (Reference Ziska and Bunce1993) suggested that an increased availability of ethylene may have been the reason for the stimulated germination they reported. Ethylene is implicated in the promotion of germination of non-dormant seeds of many species (Leubner-Metzger Reference Leubner-Metzger and Basra2006).
In different plant species, sometimes even small differences in temperature during seed development and maturation can have an influence on germination (Gutterman Reference Gutterman and Fenner2000). High temperatures during seed filling frequently disrupt normal seed development, which increases the proportion of seeds that are shrivelled, abnormal and are of lower quality (Spears et al. Reference Spears, Tekrony and Egli1997). However, it has been shown that after removal of these seeds, the germination of the remaining seeds decreases as mean maximum temperature during seed filling increases (Khalil et al. Reference Khalil, Mexal and Murray2001, Reference Khalil, Mexal, Rehman, Khan, Wahab, Zubair, Khalil and Mohammad2010; Egli et al. Reference Egli, Te Krony, Heitholt and Rupe2005; Thomas et al. Reference Thomas, Prasad, Boote and Allen2009; Table 1). High-temperature stress before the developing seeds achieve physiological or mass maturity (PM – the end of the seed filling phase) is likely to inhibit the ability of the plant to supply the seeds with the assimilates necessary to synthesize the storage compounds required during the germination process (Dornbos & McDonald Reference Dornbos and McDonald1986), and/or the seeds suffer physiological damage (see McDonald & Nelson Reference McDonald and Nelson1986; Coolbear Reference Coolbear and Basra1995; Powell Reference Powell and Basra2006) to the extent that the ability to germinate is lost.
* Day/night temperatures with 10 h at the day temperature; R5=beginning of seed fill; PM=physiological maturity; R8=harvest maturity.
† Soybean cultivars; McCall=indeterminate growth habit; Hutchenson=determinate growth habit.
‡ Seed vigour tests.
High-temperature stress after PM can also sometimes reduce germination (Green et al. Reference Green, Pinnell, Cavanaugh and Williams1965; Table 1), but more often reduces seed vigour (see next section).
The relationship between temperature during seed development and subsequent seed germination requires further investigation. For example in soybean, temperatures (32–38 °C) that reduced the germination of some cultivars in controlled environments did not vary during seed filling, in contrast to field temperatures which can vary substantially (Egli et al. Reference Egli, Te Krony, Heitholt and Rupe2005), and the plants were at these temperatures from anthesis until seed harvest. However, there may be critical periods during seed development when seeds are particularly sensitive to temperature (Egli et al. Reference Egli, Te Krony, Heitholt and Rupe2005; Shinohara et al. Reference Shinohara, Hampton and Hill2006a). This was investigated for pea (Pisum sativum L.) by Shinohara et al. (Reference Shinohara, Hampton and Hill2006a), who showed that when plants were exposed to a day/night temperature of 30/20 °C for 4 days (=240 °C h above a base temperature (Tb) of 25 °C) at the beginning of seed filling and then returned to the field until seed harvest, germination was significantly reduced in one of two cultivars (Table 2). Exposure to these conditions at later stages of seed development did not affect germination.
* S1=beginning of seed filling (810 mg/g SMC); S2=rapid seed filling (700 mg/g SMC); S3=PM (630 mg/g SMC); S4=beginning of desiccation (440 mg/g SMC); S5=harvest maturity (230 mg/g SMC); SMCs are mean of the two cultivars.
† Data are the average of 25 results in the single seed conductivity vigour test.
‡ Pea cultivars.
s.e.d. (between cultivars)=10 (mean seed weight), 5·4 (germination), 0·041 (hollow heart) and 71 (average conductivity).
While the term germination has long been used to describe the planting value of a seed lot (ISTA 2011), when conditions in the seed bed are less than optimal the germination test is a poor predictor of field emergence (Dornbos Reference Dornbos and Basra1995), suggesting that a further physiological aspect to seed quality exists – seed vigour (Powell Reference Powell and Basra2006). Seed vigour is defined by ISTA (2011) as ‘the sum of those properties that determine the activity and level of performance of seed lots of acceptable germination in a wide range of environments’, or more simply, the ability of a high germination seed lot to emerge under seed-bed stress.
While there have been reports that elevated CO2 increases or decreases seedling vigour (i.e. growth rate or biomass production) because of the effect on seed mass (Huxman et al. Reference Huxman, Hamerlynck, Jordan, Salsman and Smith1998; Steinger et al. Reference Steinger, Gall and Schmid2000), there have been no reports on the effects of elevated CO2 on seed vigour.
Seed vigour is reduced by high-temperature stress before PM (Spears et al. Reference Spears, Tekrony and Egli1997; Egli et al. Reference Egli, Te Krony, Heitholt and Rupe2005; Shinohara et al. Reference Shinohara, Hampton and Hill2006a; Table 1) and after PM (TeKrony et al. Reference TeKrony, Egli, Balles, Pfeiffer and Fellows1979, Reference TeKrony, Egli, Balles and Hebblethwaite1980; Gibson & Mullen Reference Gibson and Mullen1996; Hampton Reference Hampton, McManus, Outred and Pollock2000). Shinohara et al. (Reference Shinohara, Hampton, Hill, Juntakool, Suprakarn and Sagwansupyakorn2008) examined the relationship between vigour test results for 262 garden pea seeds lots produced in New Zealand and climate data in five regions over four consecutive production seasons, and while regional and seasonal variation for vigour occurred, these variations were significantly associated with temperature during seed development – generally the higher the temperature, the lower the seed vigour.
The susceptibility of seeds to loss of vigour following high-temperature stress depends on the stage of development (Shinohara et al. Reference Shinohara, Hampton and Hill2006a). Using hollow heart, a physiological disorder of germinating pea seeds (Halligan Reference Halligan1986) as a seed vigour indicator (Castillo et al. Reference Castillo, Hampton and Coolbear1993), Shinohara et al. (Reference Shinohara, Hampton and Hill2006a) found in a field study that hourly thermal time (HTT, measured in degree hours, °Ch, Tb=25 °C) when seeds were at the green-wrinkled pod stage (700–800 mg/g seed moisture content (SMC)) was significantly correlated with hollow heart incidence at harvest, and that 100 °Ch were required to induce the condition. There was no such relationship between HTT and hollow heart after PM. While there were cultivar differences, for one cultivar there was a linear increase in hollow heart incidence as the degree hours (°Ch) increased. In a follow-up controlled environment study, Shinohara et al. (Reference Shinohara, Hampton and Hill2006b) confirmed this result, by demonstrating that exposure to day/night temperatures of 30 and 25 °C, respectively, for 4 days (240 °Ch, Tb=25 °C) at the green-wrinkled pod stage induced hollow heart, but exposure to the same conditions at the beginning of seed fill (>800 mg/g SMC), PM (550–650 mg/g SMC) or after PM did not (Table 2). Single-seed conductivity (which is an indicator of cell membrane integrity – see Powell Reference Powell and Basra2006) was increased only after exposure of the developing seeds to the high temperature at or after PM, and not before (Table 1).
Seed vigour loss is associated with seed physiological deterioration (Powell Reference Powell1988; Hampton & Coolbear Reference Hampton and Coolbear1990), and lipid peroxidation is the most frequently cited cause (McDonald Reference McDonald1999). Lipid peroxidation causes cellular degeneration through free radical assault on important cellular molecules and structures (Wilson & McDonald Reference Wilson and McDonald1986). McDonald (Reference McDonald1999), in his model of seed deterioration, proposed four types of cell damage, viz. mitochondrial dysfunction, enzyme inactivation, membrane degradation and genetic damage.
Grass & Burris (Reference Grass and Burris1995) reported that high-temperature stress of the parent plant caused mitochondrial degeneration and reduced adenosine triphosphate (ATP) accumulation, energy levels and rates of oxygen uptake in imbibing wheat embryos (Table 3), providing clear evidence for metabolic changes at the mitochondrial level in early seed germination in response to heat stress during seed development and maturation. High temperatures during reproductive growth increase seed cell membrane damage (Nilsen & Orcutt Reference Nilsen, Orcutt, Nilsen and Orcutt1996; Shinohara et al. Reference Shinohara, Hampton and Hill2006b) so that electrolyte leakage from seeds is increased (Castillo et al. Reference Castillo, Hampton and Coolbear1994; Spears et al. Reference Spears, Tekrony and Egli1997; Shinohara et al. Reference Shinohara, Hampton and Hill2006b). High leachate conductivity in pea has been associated with dead/deteriorating tissue on the abaxial surface of the cotyledons (Powell Reference Powell, Hebblethwaite, Heath and Dawkins1985; Shinohara et al. Reference Shinohara, Hampton and Hill2006b), and on the adaxial cotyledonary surface for hollow heart (Don et al. Reference Don, Bustamante, Rennie and Seddon1984; Shinohara et al. Reference Shinohara, Hampton and Hill2006b). However, temperature stress also results in damage to the shoot apical meristem of the embryonic axis (Fu et al. Reference Fu, Lu, Chen, Zhang, Liu, Li and Cai1988; Senaratna et al. Reference Senaratna, Gusse and McKersie1988). Membrane disorganization would reduce mitochondrial efficiency and may allow the release of peroxidative enzymes capable of causing subsequent cellular damage after imbibition has begun (McDonald Reference McDonald1999).
* Day/night with 8 h day temperature and 16 h night temperature.
† AMP, adenosine monophosphate; ADP, adenosine diphosphate; ATP, adenosine triphosphate.
‡ AEC expressed as the ratio (ATP+0·5ADP/ATP+ADP+AMP)=energy status of the seed (Atkinson Reference Atkinson1968).
If heat stress leads to mitochondrial dysfunction and membrane damage, it may also result in reduced enzyme activity (e.g. decreased α-amylase – Shephard et al. Reference Shephard, Naylor and Stuchbury1996) and genetic damage (e.g. decreased DNA synthesis – Cruz-Garcia et al. Reference Cruz-Garcia, Gonzalez-Hernandez, Molina-Moreno and Vazquez-Ramos1995). Whether these and other seed deteriorative changes (see McDonald Reference McDonald1999) occur following heat stress during seed development and maturation is yet to be determined.
The environment during seed development and maturation can significantly reduce seed quality (Dornbos Reference Dornbos and Basra1995; Gusta et al. Reference Gusta, Johnson, Nesbitt and Kirkland2004; Egli et al. Reference Egli, Te Krony, Heitholt and Rupe2005; Shinohara et al. Reference Shinohara, Hampton, Hill, Juntakool, Suprakarn and Sagwansupyakorn2008), particularly seed vigour. How likely is it that elevated CO2 levels and temperature increases of up to 3 °C by 2050 will further increase this loss of seed quality? To answer this question accurately will require substantially more research in order to determine the critical periods during seed development when seeds are sensitive to environmental stresses, and for temperature, how this interacts with the duration of exposure to elevated temperatures which are deleterious to seed quality. For example, Shinohara et al. (Reference Shinohara, Hampton and Hill2006b) found that during the rapid seed filling stage in pea, a temperature of 30/25 °C for 2 days (120 °Ch at Tb=25 °C) did not induce hollow heart, but 4 days induced hollow heart in one cultivar (see Table 2), and 6 days (360 °Ch) induced the condition in both cultivars used (0·43 in cvar Alderman and 0·23 in cvar Early Onward).
From the information that is available, it can be concluded that predicted environmental changes will lead to the increased occurrence of loss of seed quality, particularly seed vigour and possibly germination. While seed mass will also change, this does not necessarily imply any negative effect on germination or vigour. To minimize the risk of reductions in seed quality the seed industry will therefore have to consider:
(a) Moving seed production to the limits of adaptation either in latitude (northern or southern) or in elevation (highland and mountainous regions) in order to reduce the chances of environmental stress (Egli et al. Reference Egli, Te Krony, Heitholt and Rupe2005; Shinohara et al. Reference Shinohara, Hampton, Hill, Juntakool, Suprakarn and Sagwansupyakorn2008).
(b) Changing sowing date so that seed filling occurs at lower temperatures (Castillo et al. Reference Castillo, Hampton and Coolbear1994; Egli et al. Reference Egli, Te Krony, Heitholt and Rupe2005; Shinohara et al. Reference Shinohara, Hampton and Hill2006a). The latter authors demonstrated that for the pea cultivar Alderman, HTT (Tb=25 °C) during the rapid seed filling stage was 198, 106 and 21 °Ch for sowings at the same site in September, October and November, respectively, and the number of hours during this stage when temperature exceeded 25 or 30 °C also reduced as sowing date was delayed (Table 4).
(c) Exploring genotypic differences in the ability to acquire and retain good seed quality in stressful environments, firstly among existing cultivars (Spears et al. Reference Spears, Tekrony and Egli1997; Shinohara et al. Reference Shinohara, Hampton and Hill2006a), and in the breeding of new cultivars (Ainsworth et al. Reference Ainsworth, Beier, Calfapietra, Ceulemans, Durand-Tardif, Farquhar, Godbold, Hendrey, Hickler, Kaduk, Karnosky, Kimball, Körner, Koornneef, Lafarge, Leakey, Lewin, Long, Manderscheid, McNeil, Mies, Miglietta, Morgan, Nagy, Norby, Norton, Percy, Rogers, Soussana, Stitt, Weigel and White2008b).
* Dates when seeds were adjudged to have reached PM.
† Period when SMC was between 700 and 800 mg/g.