Low growth temperature-induced changes to pigment composition and photosynthesis in Zea mays genotypes differing in chilling sensitivity

Authors


Pierre Haldimann Fax: 41 22 759 19 45; e-mail: HALDIMAN@UNI2 A.UNIGE.CH

Abstract

The effects on pigment composition and photosynthesis of low temperature during growth were examined in the third leaf of three chilling-tolerant and three chilling-sensitive genotypes of Zea mays L. The plants were grown under a controlled environment at 24 or 14 °C at a photon flux density (PFD) of 200 or 600 μmol m–2 s–1. At 24 °C, the two classes of genotypes showed little differences in their photosynthetic activity and their composition of pigments. At 14 °C, photosynthetic activity was considerably reduced but the chilling-tolerant genotypes displayed higher photosynthetic rates than the chilling-sensitive ones. Plants grown at 14 °C showed a reduced chlorophyll (Chl) a + b content and a reduced Chl a/b ratio but an increased ratio of total carotenoids to Chl a + b. These changes in pigment composition in plants grown at low temperature were generally more pronounced in the chilling-sensitive genotypes than in the tolerant ones, particularly at high PFD. Furthermore, at 14 °C, all the genotypes showed increased ratios of lutein, neoxanthin and xanthophyll-cycle carotenoids to Chl a + b but a reduced ratio of β-carotene to Chl a + b, especially at high PFD. At 14 °C, the chilling-tolerant genotypes, when compared with the sensitive ones, were characterized by higher contents of β-carotene and neoxanthin, a lower content of xanthophyll-cycle carotenoids, a lower ratio of xanthophylls to β-carotene, and less of their xanthophyll-cycle carotenoid pool in the form of zeaxanthin. These differences between the two classes of genotypes were more pronounced at high PFD than at low PFD. The results are discussed in terms of the relationship that may exist in maize between pigment composition and the capacity to form an efficient photosynthetic apparatus at low growth temperature.

INTRODUCTION

Chilling-sensitive plant species with a tropical/subtropical origin, like soybean (Glycine max L.) and maize (Zea mays L.), are commonly cultivated in temperate regions where prolonged periods of low temperature as well as short-term chilling events often occur in spring, during the crucial stages of germination and early vegetative growth. The ultimate consequence of such unfavourable temperature conditions will be reduced crop productivity because of a restricted planting period and delayed canopy development that can seldom be compensated for later in the season (Wolfe 1991). The delay in canopy development shown by plants grown at low temperature is accentuated by limited leaf area and chloroplast development, which greatly reduces their capacity for photosynthetic light interception even when weather conditions become favourable for growth. The thermophilic nature of maize is easily recognized if one looks in spring at field of this crop growing in a cool climate, as the plants often appear stunted with pale green, chlorotic leaves (Miedema 1982; Miedema, Post & Groot 1987).

The effects of low temperature on the physiology of maize are manifold (Miedema 1982; Stamp 1984). However, the chilling susceptibility of the photosynthetic apparatus is regarded as of particular significance (Hayden & Baker 1990; Baker 1994; Baker et al. 1994), first because maize is prone to photoinhibition of photosynthesis induced by low temperature (Long, East & Baker 1983; Ortiz-Lopez et al. 1990; Stirling et al. 1991; Nie, Long & Baker 1992; Stirling, Rodrigo & Emberru 1993; Haldimann, Fracheboud & Stamp 1996) and second because maize leaves fully developed at low temperature have a very low photosynthetic performance (Nie & Baker 1991; Nie et al. 1992; Haldimann 1996; Haldimann et al. 1996). The latter characteristic is especially likely to have consequences for photosynthetic productivity, as such leaves exhibit a sustained depression in their photosynthetic activity even at more favourable temperatures (Fryer et al. 1995; Nie et al. 1995; Haldimann 1996). It appears therefore that maize plants would benefit greatly if they were able to cope with the perturbations in development of an efficient photosynthetic apparatus induced by a low growth temperature. The photosynthetic apparatus of maize leaves grown at low temperature has been analysed in several studies (Stamp, Thiraporn & Geisler 1983; Nie & Baker 1991; Nie et al. 1992; Robertson, Baker & Leech 1993; Schapendonk, Dolstra & van Kooten 1989; Bredenkamp & Baker 1994; Haldimann, Fracheboud & Stamp 1995; Haldimann et al. 1996; Massacci et al. 1995; Haldimann 1996) but much less attention has been given to the genotypic variability that may exist in maize for the capacity to form a competent photosynthetic apparatus at low growth temperature.

It is well established that the combination of low temperature and high photon flux densities (PFDs) causes photooxidative damage (see Wise 1995). Thus, chlorosis in maize leaves is thought to occur at low temperature and high PFDs because chlorophyll is photo-oxidized before its photostable integration in the thylakoid membrane (MacWilliam & Naylor 1967). The essential function of carotenoids in protecting the photosynthetic apparatus against photo-oxidative damage has been reported many times (see reviews by Siefermann-Harms 1987; Demmig-Adams, Gilmore & Adams 1996; Yamamoto & Bassi 1996) and there is a large body of evidence that the carotenoids of the xanthophyll cycle play a dominant role in photoprotection by safely dissipating excess excitation energy that cannot be used in photosynthesis (for recent reviews see Pfündel & Bilger 1994; Demmig-Adams et al. 1996; Yamamoto & Bassi 1996; Gilmore 1997).

Recently, it has been demonstrated that growth at low temperature considerably modifies the pigment composition in maize, the large reduction in contents of chlorophylls and β-carotene being accompanied by the accumulation of large amounts of the de-epoxidized xanthophylls zeaxanthin and antheraxanthin (Haldimann et al. 1995; Haldimann 1996). In these earlier studies pigment composition was analysed in one maize genotype only. The aim of the present study was to examine the relationship between pigment composition and chilling tolerance by investigating photosynthesis and pigment composition in maize genotypes with different sensitivities to low temperature.

MATERIALS AND METHODS

Plant material and growth conditions

Six Zea mays L. inbred lines were used in the experiments: chilling-tolerant Z7 (Breeding Company Zelder, Otterersum, The Netherlands), Z15 (Breeding Company Zelder, Otterersum, The Netherlands) and KW1074 (Kleinwanzlebener Saatzucht, Einbeck, Germany) of European origin and chilling-sensitive MO17 (Experimental Station, University of Missouri, Columbia, MO, USA), CM109 and Penjalinan (Suwan Farm, Kasetsart University, Bangkok, Thailand) of tropical/subtropical origin (Stamp et al. 1983; Stamp 1984; Kocsy et al. 1996). As there are no fully chilling-tolerant cultivars of maize, the description of genotypes as chilling tolerant and chilling sensitive should be understood in the sense that within the general susceptibility of Zea mays to low temperature the first group of genotypes is much better able than the second to cope with low temperature.

Seeds were first germinated between moistened filter paper at 24 °C for 3 d. Seedlings were then planted into 1 dm3 pots (two plants per pot) containing a soil:peat mixture (5:1 by volume) and grown in growth chambers (model PGW36, Conviron, Winnipeg, Canada) at a relative humidity of 60/70% (day/night) and a photoperiod of 12 h. Light was provided by fluorescent tubes (Sylvania cool white, VHO) and incandescent bulbs (100 W, Sylvania). Two light regimens — 200 and 600 μmol photons m–2 s–1 (photosynthetically active radiation) — and two day/night temperature regimens — 24/22 °C and 14/12 °C — were used in the experiments. Plants cultivated at the low temperature regime were first grown at 24/22 °C for 5 d before the temperature was switched to 14/12 °C. All plants were grown until the full development of the third leaf (12–14 d at 24 °C and 35–45 d at 14 °C). Photosynthetically active radiation (PAR) was measured with a quantum sensor (Li-185, LiCor, Lincoln, NE, USA). Canopy temperature in the growth chamber was measured with a psychrometer (type WVU) connected to a DL2 Delta Logger (Delta T Devices Ltd, Cambridge, UK).

Measurement of photosynthesis

The net rate of CO2 assimilation (PN) was measured 6 h after the beginning of the light period using the portable photosynthesis system LiCor 6200 (LiCor, Lincoln, NE, USA) under environmental conditions equivalent to those predominating during growth.

Pigment analysis

For pigment analysis two leaf segments (1·5 cm2) were cut from the central part of the third leaf, frozen immediately in liquid nitrogen, and subsequently stored in a freezer at – 80 °C until analysis. Plant material was collected 6 h after the start of the light period. Pigment extraction and high-performance liquid chromatography (HPLC) analyses of pigments were carried out essentially according to Thayer & Björkman (1990) as described elsewhere (Haldimann et al. 1995).

Statistics

To check whether the genotypes significantly differed from each other in their photosynthetic activity and their contents of pigment, an analysis of variance of the data was made at the 5% level of significance using the STATGRAPHICS statistical system (STSC Inc., MA, USA).

RESULTS

Photosynthetic activity

At both photon flux densities (PFDs), the net rate of CO2 assimilation (PN) was similar in all the Zea mays genotypes when the plants were grown at 24 °C (Table 1). Cultivating the plants at 14 °C markedly reduced photosynthetic activity but the chilling-tolerant genotypes (Z7, Z15 and KW1074) showed a much higher PN than the chilling-sensitive ones (CM109, MO17 and Penjalinan) at both PFDs. Genotype Z15 performed best and genotype Penjalinan worst at both PFDs, PN being more than six times higher in Z15 than in Penjalinan (Table 1).

Table 1.  . Net rate of photosynthetic CO2 assimilation (PN), total chlorophyll content, chlorophyll a/b ratio, and total carotenoids content in the third leaf of three chilling-tolerant (Z7, Z15, KW1074) and three chilling-sensitive (CM109, MO17, Penjalinen) Zea mays genotypes grown at 24 °C or 14 °C under a photon flux density (PFD) of 600 μmol m–2 s–1 (high PFD) or 200 μmol m–2 s–1 (low PFD). The PN was measured under conditions equivalent to those predominating during growth. The values for PN and the pigments represent the mean of eight and five or six replications, respectively. Means for the two classes of genotypes were also calculated. Values within columns and a given growth regimen followed by the same letter are not significantly different at P < 0·05 Thumbnail image of

Chlorophylls

At 24 °C the six genotypes showed some variability in their chlorophyll (Chl) a + b content, chilling-tolerant Z15 and Z7 accumulating more Chl than the other genotypes at both PFDs (Table 1). Growth at 14 °C led generally to a large decrease in the Chl a + b content but this effect was much more pronounced in the chilling-sensitive genotypes than in the tolerant ones (Table 1). It is noteworthy that genotype Z15 retained a high Chl content at low growth temperature, so that in this genotype the Chl a + b content of plants grown at 14 °C was reduced less than 22% when compared with that of plants grown at 24 °C. By comparison, in chilling-sensitive Penjalinan the Chl content of plants grown at 14 °C was reduced by 80% (at high PFD) or 70% (at low PFD) when compared with that of plants grown at 24 °C (Table 1). At 24 °C, the Chl a/b ratio was comparable for the six genotypes but higher at high PFD than at low PFD (Table 1). At both PFDs, growth at 14 °C resulted in a marked decrease in the Chl a/b ratio, which was more pronounced in the chilling-sensitive genotypes than in the tolerant ones at high PFD.

Total carotenoids pool

The total carotenoids content was expressed in relation to unit leaf area as well as Chl a + b because, as pointed out for sun leaves and shade leaves (Logan et al. 1996), acclimatory differences in leaf thickness between plants grown at 24 °C and those grown at 14 °C influence the relationship between content of pigment and leaf area. At 24 °C, the total carotenoids content, expressed in relation to unit leaf area, was similar in KW1074, CM109, MO17 and Penjalinan but higher in Z7 and Z15 at both PFDs (Table 1). The six genotypes displayed less marked differences in their carotenoids content when it was expressed in relation to Chl a + b, but in this case the carotenoids content was higher in the three chilling-tolerant genotypes than in the three tolerant ones at low PFD. In all the genotypes the total carotenoids/Chl a + b ratio was higher at high PFD than at low PFD (Table 1). At both PFDs, growth at 14 °C led to a decrease in the total carotenoids content in relation to unit leaf area in the chilling-sensitive genotypes (Table 1). In contrast, in the chilling-tolerant genotypes the total carotenoids generally changed little (KW1074 and Z7) or even increased (Z15) in response to growth at low temperature, with the exception of a reduced carotenoid content in Z7 at low PFD (Table 1). As, when compared with the Chl a + b content, the total carotenoids content was affected much less, if at all, by low growth temperature, the ratio of total carotenoids to Chl a + b was much higher at 14 °C than at 24 °C, especially at high PFD (Table 1). Furthermore, at high PFD, this ratio was higher in the three chilling-sensitive genotypes and chilling-tolerant Z7 than in chilling-tolerant Z15 and KW1074 (Table 1).

Carotenoid composition

Contents of the different components of the carotenoids pool were expressed in relation to Chl a + b (Table 2) and as a mol percentage of the total carotenoids content (Table 3), as these modes of expression allow a better comparison of the carotenoid composition of the different genotypes. At 24 °C, irrespective of the mode of expression, the β-carotene content was higher at high PFD than at low PFD but the genotypic variability for this trait was rather limited, even if the β-carotene to Chl a + b ratio was higher in the chilling-tolerant genotypes than in the tolerant ones (Tables 2 & 3). In most of the genotypes growth at 14 °C led to a reduction in the ratio of β-carotene to Chl a + b (Table 2). This effect became particularly apparent when the β-carotene content was expressed as a mol percentage of the total carotenoids pool (Table 3). Furthermore, at 14 °C and high PFD, the portion of β-carotene was much lower in the chilling-sensitive genotypes than in the tolerant ones (Table 3). At 24 °C, irrespective of the mode of expression, the six genotypes showed little differences in their contents of lutein and total xanthophyll-cycle carotenoids [violaxanthin (V) + antheraxanthin (A) + zeathanthin (Z)] but the V + A + Z content was higher at high PFD than at low PFD (Tables 2 & 3). Interestingly, at 24 °C, the neoxanthin content was higher in the chilling-tolerant genotypes than in the sensitive ones at both PFDs (Tables 2 & 3). Mainly because of the decrease in the chlorophyll content induced by low temperature, the ratios of lutein, neoxanthin and V + A + Z to Chl a + b were much higher at 14 °C than at 24 °C (Table 2). This observation especially holds true at high PFD for the chilling-sensitive genotypes. However, expressing the contents of the different carotenoids as a percentage of total carotenoids content revealed that the decrease in β-carotene content induced by low temperature was accompanied by a large increase in the content of V + A + Z (especially at high PFD), while the relative contents of lutein and neoxanthin were affected by growth at 14 °C to a much lesser extent, if at all (Table 3). The increase in the proportion of V + A + Z relative to the total carotenoids pool was generally more pronounced in the chilling-sensitive genotypes than in the tolerant ones, so that in chilling-sensitive Penjalinan and CM109 V + A + Z accounted for more than 50% of the total carotenoids pool at high PFD (Table 3). It is noteworthy, however, that the proportion of V + A + Z was also comparatively high in chilling-tolerant Z7.

Table 2.  . Carotenoid composition expressed in relation to chlorophyll in the third leaf of three chilling-tolerant (Z7, Z15, KW1074) and three chilling-sensitive (CM109, MO17, Penjalinen) Zea mays genotypes grown at 24 °C or 14 °C under a photon flux density (PFD) of 600 μmol m–2 s–1 (high PFD) or 200 μmol m–2 s–1 (low PFD). All the values represent the mean of five or six replications. Means for the two classes of genotypes were also calculated. Values within columns and a given growth regimen followed by the same letter are not significantly different at P < 0·05. V, violaxanthin; A, antheraxanthin; Z, zeaxanthin Thumbnail image of
Table 3.  . Carotenoid composition expressed as a percentage of the total carotenoids content and the xanthophylls to β-carotene ratio (X/C) in the third leaf of three chilling-tolerant (Z7, Z15, KW1074) and three chilling-sensitive (CM109, MO17, Penjalinen) Zea mays genotypes grown at 24 °C or 14 °C under a photon flux density (PFD) of 600 μmol m–2 s–1 (high PFD) or 200 μmol m–2 s–1 (low PFD). All the values represent the mean of five or six replications. Means for the two classes of genotypes were also calculated. Values within columns and a given growth regimen followed by the same letter are not significantly different at P < 0·05. V, violaxanthin; A, antheraxanthin; Z, zeaxanthin Thumbnail image of

The ratio of xanthophylls to β-carotene was higher at low PFD than at high PFD in plants grown at 24 °C but the genotypic variability was limited (Table 3). Growth at 14 °C led to a large increase in the ratio of xanthophylls to β-carotene, especially at high PFD. Furthermore, at high PFD this ratio was much higher in the chilling-sensitive genotypes than in the tolerant ones, whereas at low PFD the two types of genotypes showed less clear differences for this trait.

As at 24 °C the V + A + Z pool was mainly in the form of violaxanthin, trace amounts of antheraxanthin and zeaxanthin being present only at high PFD (data not shown), details on the composition of the V + A + Z pool are given only for 14 °C-grown plants (Table 4). It appeared that in the chilling-sensitive genotypes zeaxanthin accounted for about 85% of the V + A + Z pool at high PFD, whereas the proportion of zeaxanthin was only 56% (Z7) or much less (Z15 and KW1074) in the chilling-tolerant genotypes at the same PFD. At low PFD the fraction of zeaxanthin was much lower and the difference between the two types of genotypes less pronounced. The chilling-tolerant genotypes displayed a higher fraction of antheraxanthin than the sensitive ones at high PFD (Table 4).

Table 4.  . Composition of the xanthophyll-cycle carotenoids in the third leaf of three chilling-tolerant (Z7, Z15, KW1074) and three chilling-sensitive (CM109, MO17, Penjalinen) Zea mays genotypes grown at 14 °C under a photon flux density (PFD) of 600 μmol m–2 s–1 (high PFD) or 200 μol m–2 s–1 (low PFD). All the values represent the mean of five or six replications. Means for the two classes of genotypes were also calculated. Values within columns and a given growth regimen followed by the same letter are not significantly different at P < 0·05 Thumbnail image of

DISCUSSION

When grown at 24 °C, the six genotypes of Zea mays showed generally few differences in their photosynthetic activity, their Chl a/b ratio, their ratio of total carotenoids to Chl a + b (Table 1) and their carotenoid composition (Table 3), while the contents of Chl a + b and total carotenoids, expressed in relation to unit leaf area, were higher in chilling-tolerant Z7 and Z15 than in the other genotypes (Table 1). These results indicate that there is no intrinsic major difference in pigment composition between the two classes of genotypes. However, the neoxanthin content was higher in the chilling-tolerant genotypes than in the sensitive ones at both PFDs (Table 3). What might be the physiological meaning of such a difference in the content of neoxanthin between the two types of genotypes remains an open question, as a specific role for neoxanthin has not yet been described. The finding that, at 24 °C, the Chl a/b ratio, the total carotenoids content (Table 1) and the contents of β-carotene and xanthophyll-cycle carotenoids (V + A + Z) (Tables 2 & 3) were higher at high PFD than at low PFD reflects an adaptation of the photosynthetic apparatus to the light environment and is consistent with the results obtained in other studies (e.g. Haldimann et al. 1995; Logan et al. 1996).

More important, however, are the marked differences in chilling susceptibility between the two categories of genotypes demonstrated when the plants experienced low temperature (14 °C) during growth, the chilling-tolerant genotypes being clearly much better able to cope with depressions in photosynthetic activity induced by low growth temperature than were the chilling-sensitive ones at both PFDs (Table 1). The higher photosynthetic activity of the chilling-tolerant genotypes at low temperature generally correlated with their ability to retain higher amounts of chlorophylls and total carotenoids than the chilling-sensitive genotypes, in which the chlorophyll content was very low, particularly at high PFD (Table 1). This observation confirms the finding that within the species Zea mays there is a large genotypic variability with regard to resistance to low-temperature-induced chlorosis (Stamp et al. 1983; Stamp 1987). If pigment content can be considered indicative of the amount of photosynthetic apparatus, the higher photosynthetic activity of the chilling-tolerant genotypes is likely to be based on their ability to develop more photosynthetic apparatus per unit leaf area at low growth temperature than the chilling-sensitive genotypes. However, it has to be emphasized that the higher pigment content of the chilling-tolerant genotypes compared with that of the sensitive ones is probably also partly related to the thicker leaves developed by the former genotypes at low growth temperature.

As well as reducing the amount of photosynthetic apparatus, growth of maize at suboptimal temperature has been shown to induce modifications to the thylakoid composition in mesophyll and bundle sheath cells, a number of polypeptides encoded by the chloroplast genome failing to accumulate at low growth temperature (Nie & Baker 1991; Robertson et al. 1993; Nie et al. 1995). The xanthophylls (including neoxanthin and lutein) are mainly associated with polypeptides of the light-harvesting antenna complexes of photosystem I (PSI) and photosystem II (PSII) that are encoded by the nuclear genome, while β-carotene is mainly associated with polypeptides of the reaction-centre cores of PSI and PSII that are encoded by the chloroplast genome (Lee & Thornber 1995; Yamamoto & Bassi 1996). Furthermore, PSI and PSII light-harvesting antenna complexes are known to contain Chl a and Chl b molecules, while only Chl a is present in the reaction-centre cores of PSI and PSII (see Yamamoto & Bassi 1996). Thus, as suggested previously (Nie & Baker 1991; Haldimann et al. 1995), the low β-carotene content (Tables 2 & 3), the reduced Chl a/b ratio (Table 1), the unchanged relative contents of lutein and neoxanthin (Table 3) as well as the increased ratio of xanthophylls to β-carotene (Table 3) observed in maize leaves grown at low temperature most probably mirror the reduced proportion of reaction-centre core complexes relative to light-harvesting complexes in these leaves (see Nie & Baker 1991). The high content of xanthophyll-cycle carotenoids observed in leaves grown at suboptimal temperature (Tables 2 & 3) might also be indicative of a different organization of PSII complexes and perhaps also PSI complexes in leaves grown at low temperature compared with those grown at normal temperature, as xanthophyll-cycle carotenoids have been shown to be mainly associated with minor pigment–protein complexes (Bassi et al. 1993). As it has been shown that large amounts of β-carotene are associated with PSI and that PSI exhibits a high Chl a/b ratio (Thayer & Björkman 1992), it is also possible that low-growth-temperature-dependent changes of the β-carotene content (Tables 2 & 3) and the Chl a/b ratio (Table 1) reflect changes in the stoichiometry between PSI and PSII. The above-described modifications of pigment composition induced by low growth temperature were generally more pronounced in the chilling-sensitive genotypes than in the tolerant ones at high PFD, whereas at low PFD the two types of genotypes showed less marked, if any, differences for these traits. Thus, enhancement of low-temperature-induced perturbations of chloroplast development by a high PFD and perhaps a more general susceptibility to light stress at low temperature appear to be additional factors responsible for the inability of the chilling-sensitive genotypes to achieve photosynthetic competence at low growth temperature.

The large increase in the ratio of total carotenoids to Chl a + b that occurred in all genotypes in response to growth at low temperature and was more pronounced at high PFD than at low PFD (Table 1) can be considered to reflect an adaptation strategy of the plants that allows them on the one hand to reduce light absorption and on the other to increase the capacity for photoprotection. Moreover, the substantial increase in the content of the carotenoids of the xanthophyll cycle (V + A + Z) (Tables 2 & 3), associated with the accumulation of large amounts of the de-epoxidized xanthophylls zeaxanthin and antheraxanthin (Table 4), most probably occurred in maize plants grown at low temperature to increase the capacity to dissipate absorbed excitation energy that cannot be used in photosynthesis or dissipated in alternative pathways. Accumulation of zeaxanthin in maize leaves grown at low temperature has been observed in earlier studies (Haldimann et al. 1995;1996; Fryer et al. 1995; Haldimann 1996) and zeaxanthin-related dissipation of absorbed excitation energy at PSII has been shown to be the most important factor responsible for the reduced photosynthetic efficiency in maize plants grown at low temperature (Fryer et al. 1995). Likewise, from studies using cold-tolerant plant species it has been reported that low-temperature-dependent sustained depressions in photochemical efficiency of PSII are mainly, if not fully, related to a down regulation of PSII that involves sustained xanthophyll cycle-associated energy dissipation (Adams & Demmig-Adams 1994, 1995; Adams, Hoehn & Demmig-Adams 1995a; Adams et al. 1995b; Verhoeven, Adams & Demmig-Adams 1996). However, it should be emphasized here that low-temperature-dependent reductions in photochemical efficiency of PSII have also been related to altered PSII reaction centres (Krause 1994; Fryer et al. 1995; Ottander, Campbell & Öquist 1995).

With regard to the role of the xanthophyll cycle in photoprotection the finding that, compared with the chilling-tolerant genotypes (with the exception of genotype Z7), the chilling-sensitive ones exhibited a larger V + A + Z pool (Tables 2 & 3) and had a more important part of their V + A + Z pool in the form of zeaxanthin at both PFDs (Table 4) is probably related to the higher requirement for dissipation of absorbed excitation energy of the chilling-sensitive genotypes because of their low photosynthetic performance (Table 1). Interestingly, the proportion of antheraxanthin within the V + A + Z pool was higher in the chilling-tolerant genotypes than in the sensitive ones at 14 °C and high PFD (Table 4). However, if as proposed in the literature (Gilmore & Yamamoto 1993; Demmig-Adams & Adams 1996), antheraxanthin has a similar function to zeaxanthin in photoprotection, the difference in the relative content of antheraxanthin between the two types of genotypes appears not to be of major significance.

In conclusion, when chilling-tolerant and chilling-sensitive maize genotypes experience low temperature during growth, differences in pigment content and composition develop that reflect the chilling-tolerant genotypes’ superior ability to cope with the low-temperature-induced perturbations in chloroplast development which are responsible for the low photosynthetic performance of maize leaves developed at low temperature.

Acknowledgements

I thank Dr S. S. Thayer (Carnegie Institution of Washington, Stanford, CA, USA) for helpful advice on HPLC analysis of pigments.

Footnotes

  1. Present address: Laboratory of Bioenergetics, University of Geneva, 10 chemins des Embrouchis, CH-1254 Jussy-Lullier/GE, Switzerland.

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