Growth and development of maize (Zea mays L.) seedlings under chilling conditions in the field

Growth and development of maize (Zea mays L.) seedlings under chilling conditions in the field

European Journal of Agronomy European Journal of Agronomy 5 (1996) 31-43 Growth and development of maize (Zea ways L.) seedlings under chilling condi...

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European Journal of Agronomy European Journal of Agronomy 5 (1996) 31-43

Growth and development of maize (Zea ways L.) seedlings under chilling conditions in the field M.J. Verheul, C. Picatto, P. Stamp * Institut fiir Pfanzenwissenschaften, Eidgeniissische Technische Hochschule (ETH), CH-8092 Ziirich, Switzerland

Universitiitstrasse 2,

Accepted 3 January 1996

Abstract Maize inbred lines of different origins were grown in spring (for 2 years at early and usual sowing dates) in northeastern Switzerland (latitude 47”27’ N; 550 and 720 m a.s.1.) until five to six leaves were fully developed. Averaged over all observation periods, the group of inbred lines used in hybrids for cool temperate regions (CT lines) showed better heterotrophic and autotrophic shoot growth and faster development than the group of lines adapted to warm tropical regions (CS lines). The more efficient autotrophic shoot growth of CT lines was expressed by higher rates of relative growth (RGR) and relative leaf area expansion (RLGR) and was related to a higher net assimilation rate (NAR) and a lower leaf area ratio (LAR). CT lines had better radiation use efficiency (RUE), higher rates of net photosynthesis (PN), and lower specific leaf area (SLA) than CS lines. The greater RGR and RLGR of CT line Z 7 as compared to the CS line Penjalinan were related to a higher assimilation rate but not to a better use of carbohydrates; in Z 7 the balance between assimilation production and use resulted in a greater accumulation of soluble carbohydrates and starch. Genotypic variability existed for most growth parameters and was greatest for NAR. Growth responses of inbred lines under field conditions in spring were influenced mainly by temperature. Of all parameters, NAR was correlated best with temperature. Under decreasing temperature, RGR, RLGR, the rate of leaf appearances (RLA) and NAR decreased, whereas LAR, leaf area partitioning (LAP), and SLA increased slightly. The soluble carbohydrate content of Z 7 and Penjalinan also increased. RUE showed the best correlation with the daily minimum air temperature. Within the temperature limits of this experiment, no significant interactions were found between inbred line and temperature. Keywords: Maize (Zea mays L.); Chilling

Photosynthesis;

Soluble carbohydrate

tolerance;

1. Introduction

Early growth of thermophilic maize plants is limited by temperatures below 15°C (Alberda, 1969; Castleberry et al., 1978; Stamp, 1984). At

* Corresponding author.

Inbred

lines; Growth

Dry matter

accumulation;

suboptimal temperatures in the field during spring result in decreased crop productivity (Carr and Hough, 1978; te Velde, 1986) and poor yield stability (Stamp, 1986). Improvement of chilling tolerance should lead to a higher growth rate and thus to a more rapid development of ground cover, enabling maize plants to be more competi-

high latitudes,

tive with weeds and reducing

1161-0301/96/$15.00Copyright 0 1996Elsevier Science B.V. All rights reserved PZZ S1161-0301(96)02007-2

analysis;

content

unfavourable

envi-

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M. J. Verheul et al.lEuropean Journal of Agronomy 5 (1996) 31-43

ronmental side effects of maize cultivation such as soil erosion, nitrate leaching, and the need for the intensive use of herbicides (Aufhammer, 1985). Furthermore, a more rapid development of ground cover would result in greater light interception throughout the growing season, and through an earlier grain-filling period crop productivity could be increased (Mock and Skrlda, 1978). A rational approach to breeding for cold tolerance requires a description of plant features which limit maize growth under low temperatures and an estimation of the genetic variability of those features (Miedema, 1982). Responses of maize to chilling stress have been reviewed by several authors (Miedema, 1982; Crevecoeur and Ledent, 1984; Stamp, 1984, 1986; Bochicchio, 1985; Miedema et al., 1987). All studies emphasise the complex reactions of the plant to various chilling events. Low temperatures can have different effects on germination (Zemetra and Cuany, 1991) emergence (Blacklow, 1972), and heterotrophic (Giauffret and Derieux, 1991) and early autotrophic plant growth (Alberda, 1969; Hardacre and Eagles, 1979). In young plants, chilling tolerance can include survival during and after a severe stress (0-6°C) and maintenance of growth processes under mild chilling stress (lo-15’C) (Stamp, 1984). Field experiments have focused on early seedling growth, i.e., seed germination, rate of emergence, and heterotrophic growth (Mock and Skrlda, 1978; Mock and McNeil, 1979). Autotrophic growth of young maize plants, which begins after the development of the third leaf (Barloy, 1984), has received little attention. Improving growth performance during this stage may, however, be essential for increasing dry matter yield and yield stability (Dolstra and Miedema, 1986). Temperature can affect dry matter accumulation through its effect on the photosynthetic capacity per unit leaf area and on the size of the leaves. At chilling temperatures, shoot growth processes may be limited by a decreased amount of assimilates (source limitation) or a decreased leaf area expansion (sink limitation). Berry and Raison (1981) suggested that differences in growth responses to temperature in maize are dominated by the to temperature. response of photosynthesis

Additional damage of the photosynthetic apparatus of maize can occur at low temperature and high light intensity (Baker et al., 1988). Rates of leaf initiation (Tollenaar et al., 1979) and leaf elongation (Miedema et al., 1987) show curvilinear responses to temperature with a minimum at 7°C and a maximum at approximately 31°C. The accumulation of carbohydrates in chilled plants (Grobbelaar, 1963; Brouwer et al., 1973; Pollock and Eagles, 1988) and the observation that leaf area expansion is much more affected by low temperatures than is shoot dry matter accumulation (Milthorpe, 1959; Miedema and Sinnaeve, 1980; Stamp, 1981; Crevecoeur and Ledent, 1984) have led to the assumption that the effects of temperature on dry matter production are associated with the growth of the leaves rather than with net photosynthesis (Duncan and Hesketh, 1968; Hanson, 1971; Miedema, 1982; Pollock, 1990). Growth analysis is an important first step in an analysis of morphological, physiological, or biochemical factors determining relative growth rate (RGR) (Lambers, 1987). During early phases of development, dry matter partitioning to leaf area has, potentially, a strong impact on crop growth, since variations in leaf area index (LAI) will have a direct impact on the rate of dry matter accumulation (Tollenaar, 1989). A decrease in leaf area ratio (LAR) with decreasing temperature and a consequent reduction in RGR are often linked to morphological adaptation, especially a decrease in specific leaf area (SLA) (Beauchamp and Lathwell, 1966; Acock et al., 1979). In field studies, dry matter production of the maize crop is often linearly related to the amount of absorbed photosynthetically active radiation (PAR) (Kiniry et al., 1989; Schapendonk et al., 1994). During early growth, the use of intercepted light for dry matter production, assessed by the ratio between both parameters and defined as the radiation use efficiency (RUE) (Bonhomme et al., 1982), was reported to be only a third of that just before silking (Varlet-Grancher et al., 1982; Giauffret et al., 1991; Schapendonk et al., 1994). Temperature did not appear to affect RUE in plants not subjected to chilling stress (Kiniry et al., 1989). However, RUE in maize grown in regions characterised by a cool spring ( 15- 18°C) was lower

M. J. Verheul et al./European Journal of Agronomy 5 ( 1996) 31-43

than the RUE reported for maize grown in warmer regions (Andrade et al., 1992). An additional problem in studying mechanisms of chilling tolerance is that the results of field trials and growth chamber trials are difficult to compare, as illustrated by the generally poor correlations between the two environments (Miedema et al., 1987). Under field conditions, seedlings are rarely stressed by long periods of constantly low temperatures. In this study, the early autotrophic shoot growth and development of maize inbred lines of different origins were investigated under field conditions in spring. An analysis of growth (following Hunt, 1978) was made to quantify growth reactions and to evaluate environmental effects on leaf area expansion, biomass partitioning within the shoot, and carbon assimilation in relation to the total dry matter production.

2. Materials and methods 2.1. Plant material and growing conditions To investigate seedling growth and development under field conditions, three inbred lines of Zea mays L. (KW 1074, Z 7, and Z 15), which were adapted to cool temperate regions (CT), and three inbred lines (Penjalinan, MO 17, and CM 109) used in breeding programmes in warm tropical regions (CS) were grown in the northeastern part of Switzerland (latitude 47”27’N) at two altitudes (550 and 720 m a.s.1.)for 2 years. Seeds were sown on dates customary for this region and earlier (Table 1) in randomised blocks with six replications. Individual lines were grown in plots of one row, 6 m long. The distance between rows was 75 cm. Seeds were sown at depths of 4-5 cm at intervals of 15 cm, giving a plant density of 9 plants m-‘. In the course of the trials, plants were harvested so as to reduce mutual plant shading. Fertiliser (90 kg ha-’ P,05 and 180 kg ha-’ KzO) was ploughed under before sowing; 90 kg ha- ’ N were applied after emergence. Weeding was done mechanically. Snails were controlled by applying 1 kg ha-’ Limax (Maag AG Dielsdorf, containing 6% metaldehyde). All seeds were treated

33

with Gamasat (Maag AG Dielsdorf, active compounds: 50% thiram, 8% captan, 20% lindane). During the trials, mean daily air temperatures, calculated as the averages of continuously recorded temperatures each 24 h, were usually in the range at which mild (lo-15C) chilling stress in maize occurs (Table 1). Minimum air temperature was occasionally in the range at which severe chilling stress (0-6°C) may occur. Mean soil temperature, measured at a depth of 5 cm, followed the same pattern as the mean air temperature but was higher. Averaged over all observation periods, the mean daily air temperature was 14.O”C and the mean daily soil temperature 16.9”C. 2.2. Plant sampling and growth analysis Vegetative shoot mass was determined weekly when one, three, four, and five leaves were fully expanded (Table 1). Plants were usually harvested just after a cold or a warm period. Shoots of five plants per plot were cut off at the coleoptilar node. Visible leaf blades were cut off; the rest (mainly leaf sheaths and non-exposed leaf tissue tightly wrapped within the stem axis) was designated as ‘stem’. Leaf area was measured with an area meter (LICOR LI-3100). Leaves and stems were dried for 72 h at 65°C and then weighed. RGR, NAR (net assimilation rate), LAR, SLA (specific leaf area), and leaf weight ratio (LWR) of plant shoots were calculated according to Hunt ( 1978). Relative leaf area growth rate (RLGR) and leaf area partitioning (LAP) were calculated according to Potter and Jones (1977). The relationships between these parameters (RGR = NAR x LAR, LAR = SLA x LWR and RLGR = NAR x LAP) provide a useful framework for interpreting results (Hunt, 1982; Poorter, 1989). The rate of leaf appearance (RLA), defined as the frequency with which leaves become visible within the uppermost whorl of leaves, was calculated to describe the developmental aspect of growth. RGR was calculated as the slope of the relation between the In dry weight and chronological time between two successive harvests. RGR of individual lines, calculated during observation periods after the development of the third leaf, were averaged over all treatments (sowing dates, loca-

M. J. Verheul et al.lEuropean

34

Journal of Agronomy

5 (1996) 31-43

Table 1 mean soil (Tsoi,) temperature, global radiation (GR), Daily mean (Ta,mean)) minimum (T.,,,,), and maximum (T,,,,, ) air temperatures, and precipitation (P). averaged over observation periods following early and usual sowing dates at low (550 m a.s.1.) altitude and a usual sowing date at high (720 m a.s.1.) altitude. The developmental stage gives the number of fully developed leaves at beginning and end of observation period

Early sowing

Sowing date

Observation period

Developmental stage

K,,,,, (“C)

L,rn (“C)

Ta.max (“C)

‘Lt (“C)

GR (MJ mm2 d-‘)

P (mm d-r)

25 April 89

22 May-02 June 2 June-15 June 15 June-23 June 15 May-27 May 27 May-05 June OS Junee12June 12June-22 June 25 May-08 June 08 June-16 June 16 June-24 June 03 June-19 June 19 June-27June 27 June-03 July 25 May-08 June 08 June-16 June 16 June-24June

1.0+2.7 2.7+3.9 3.9+5.4 1.0+2.8 2.8-+3.6 3.6+4.2 4.2-5.5 l.Od2.3 2.343.5 3.5+5.0 1.0+3.0 3.Oh4.4 4.4d5.2 1.0+2.4 2.4-3.4 3.4+4.9

15.1 12.9 16.4 14.4 12.7 11.0 14.6 12.6 15.8 16.4 12.7 16.5 16.6 11.6 15.1 15.4

9.8 7.8 10.5 9.2 6.7 8.1 8.6 8.0 9.6 10.8 8.3 10.9 11.7 6.2 8.6 8.9

21.5 18.0 22.9 19.9 17.7 14.5 20.0 17.5 21.6 22.8 17.0 22.1 22.1 17.9 21.7 21.5

17.8 15.5 20.2 16.4 15.2 14.4 17.0 15.7 18.0 19.8 15.6 18.3 19.7 15.1 18.6 19.1

20.9 22.2 23.1 20.0 19.8 11.9 19.2 18.9 25.6 21.9 15.7 19.9 17.2 16.4 22.8 19.1

3.1 2.5 1.5 2.7 5.9 8.0 3.7 3.9 0.9 1.5 5.1 1.5 4.3 3.6 0.5 1.4

26 April 90

Usual sowing

08 May 89

17 May 90

High elevation

08 May 89

tions, and years) to describe mean relative growth rates during early autotrophic growth. As a test of exponential growth, the linear regression of In dry weight and time was calculated. High correlation coefficients (u> +0.9) were found in all individual lines, which justified comparisons among lines (Hunt, 1982). The photosynthetically active radiation (PAR) intercepted by the crop (G) was estimated according to Bonhomme et al. (1982): G=0.46 x Go (1-exp (-0.7 x LAI). Global solar radiation (G,) was recorded daily. The leaf area index (LAI) was assessed using leaf area measurements at each harvest. Radiation use efficiency (RUE, g MJJ’ PAR) was calculated as the ratio of the accumulated dry weight to the total intercepted PAR between two successive harvests. 2.3. Net photosynthesis Net photosynthesis (PN) was measured, using a portable photosynthesis system (LICOR-6200, LICOR, Lincoln, Nebraska), on 3 days in the field trial sown on 26 April 1990. P, was measured on the central part of the fourth leaf of nine plants of

each inbred line on 29 May, 10 June, and 16 June between 10:00 and 12:00 h. Leaf temperatures and light intensities were 20°C and 1200 pm01 mp2 s- i, 26°C and 1900 umol me2 s-i, and 27°C and 1580 umol me2 s-i, respectively. 2.4. Analysis of soluble carbohydrates and starch Dried plant material was ground to pass through a OS-mm sieve. Soluble carbohydrates (from aliquots of 50-60 mg) were extracted in 5 cm3 80% ethanol for 30 min at 60°C; the aliquots were stirred constantly. After centrifugation the supernatant was collected, and extraction was repeated as described above. Soluble carbohydrates in the collected extracts were determined using the anthrone method (Seifter et al., 1950; Mercier and Tollier, 1982). An aliquot of the extract was hydrolysed in 4 cm3 anthrone solution (2 g ll’ anthrone, 70% H2S04) in a boiling water bath for 15 min. After cooling, the carbohydrate concentration was determined spectrophotometrically at 620 nm. Glucose was used as a standard. Starch in the residue was released in 3 cm3 water

M.J. Verheul et al./European Journal of Agronomy 5 (1996) 31-43

with termamyl (heat stable a-amylase, 7 ml termamy1 120 kNul-’ H,O) for 20 min in a boiling water bath. After cooling to room temperature, 2 cm3 NaOH-buffer (pH 4.6) were added. Starch was hydrolysed by adding an enzyme solution (amyloglucosidase, Boehringer No. 208469); samples were then put into a water bath for 30 min at 60°C and stirred constantly. After filling to 25 cm3 with water, the suspension was filtered. The released glucose was assayed with hexokinase and glucose6-phosphate-dehydrogenase and measured spectrophotometrically at 340 nm (Anonymous, 1987). 2.5. Statistics Growth parameters of six inbred lines were determined for two altitudes, two sowing dates, and four to five harvest dates for 2 years, thus giving 16 observation periods (Table 1). On each harvest date, samples of five plants per inbred line and replication were harvested. When comparing autotrophic growth of lines, data of 13 observation periods was used. An analysis of variance was taking the 5% level of significance using the STATGRAPHICS statistical graphics system, version 4.0 (STSC Inc., Maryland, USA). Correlations between growth parameters and between environmental conditions and growth parameters were based on 13 observation periods and six genotypes (78 observations, unless stated otherwise).

3. Results 3.1. Growth analysis and genotypic variability of growth parameters

3.1.1. Heterotrophicplant growth Plant growth was considered to be heterotrophic until three leaves were fully developed (Stamp, 1984). The third leaf was fully developed 42 and 36 days after sowing on the early and usual sowing dates in 1989. In 1990, full development of the third leaf was reached at 34 and 33 days after sowing. The accumulated dry matter and leaf area at this stage tended to be greater in CT lines than in CS lines (Table 2) indicating a faster heterotrophic plant growth of CT lines under the given

35

Table 2 Dry matter and leaf area per plant at the end of heterotrophic growth of maize inbred lines (KW 1074, Z 7, and Z 15) adapted to cool temperate regions (CT) and of maize inbred lines (Penjalinan, MO 17, and CM 109) used in breeding programmes in warm tropical regions (CS) at full expansion of the third leaf Inbred line

KW 1074 z 15 27 Penjalinan MO 17 CM 109 CT CS Mean cv (%)

Dry matter

Leaf area

(mg)

(+ SE)

(cm’)

(*SE)

278 304 382 247 171 238 321 219 270 26.3

84 73 74 113 48 59 89 86

69 63 90 70 41 57 74 56 65 24.9

27 21 25 42 13 19 27 30

The values are means (k SE: standard error of mean) across five environments and six replications (n=30). CV, coefficient of variation.

temperature conditions. Considerable genetic variation in heterotrophic growth was found in the lines under investigation. This variation may have been due to differences in the amount of kernel reserves in these lines. However, no correlation was found between seed weight and dry matter or leaf area at this developmental stage (data not shown). 3.1.2. Autotrophicplant growth After the third leaf was fully expanded, growth was considered to be autotrophic. Autotrophic plant growth was measured until five to six leaves were fully developed (Table 1). Averaged over all observation periods, CT lines had a significantly greater RGR than CS lines (Table 3). This was associated with a significantly greater RLGR and NAR. Thus, under the low temperature conditions in this experiment (Table l), the more efficient dry matter accumulation of CT lines was related to faster leaf growth and to more efficient production of dry matter per unit leaf area. Moreover, the greater RGR of CT lines was related to a significantly greater RUE. CT lines showed efficient dry matter accumulation in spite of an unfavourable morphology. CT lines had a significantly lower

M. J. Verheul et al./European Journal of Agronomy 5 (1996) 31-43

36

Table 3 Mean relative growth rates (RGR), relative leaf area growth rates (RLGR), net assimilation rates (NAR), leaf area ratios (LAR), specific leaf areas (SLA), leaf weight ratios (LWR), leaf area partitioning (LAP), rates of leaf appearance (RLA), and radiation use efficiency (RUE) of young autotrophic maize plants under field conditions in spring Inbred

line

RLGR (m’ m-’ day-‘)

RGR (gg-’ day-‘)

KW 1074 2 15 27 Penjalinan MO 17 CM 109 CT cs Mean cv (%)

0.133 0.133 0.133 0.108 0.114 0.124 0.133 0.115 0.124 8.8

(a) (a) (a) (b) (b) (ab) (a) (b)

0.123 0.122 0.118 0.091 0.104 0.106 0.121 0.100 0.111 11.3

NAR (gm-’ day-‘) (a) (a) (a) (b) (ab) (ab) (a) (b)

5.75 7.07 6.29 4.46 5.00 5.70 6.37 5.05 5.71 16.1

(abc) (a) (ab) (c) (bc) (abc) (a) (b)

LAR (cm’

SLA (cm’

g-‘)

g-i)

241 (ab) 200 (c) 220 (bc) 257 (a) 240 (ab) 231 (abc) 221 (b) 243 (a) 232 8.5

329 (ab) 250 (d) 299 (bc) 334 (a) 319 (abc) 285 (c) 293 (b) 313 (a) 303 10.5

LWR

0.733 0.797 0.733 0.773 0.748 0.804 0.754 0.775 0.765 4.1

LAP (cm2

(b) (a) (b) (ab) (b) (a) (a) (b)

g-i)

RLA (leaves day-‘)

219 (a) 177 (b) 188 (ab) 207 (ab) 215 (a) 188 (ab) 195 (a) 204 (a) 199 8.5

0.166 0.125 0.142 0.125 0.123 0.144 0.144 0.131 0.138 12.2

RUE (g MJJ’ PAR) (a) (b) (ab) (b) (b) (ab) (a) (a)

0.84 1.03 0.93 0.69 0.71 0.84 0.94 0.75 0.84 15.4

(abc) (a) (ab) (c) (bc) (abc) (a) (b)

Three inbred lines (KW 1074, Z 7, and Z 15) adapted to cool temperate regions (CT) and three lines (Penjalinan, MO 17, and CM 109) adapted to warm tropical regions (CS) were used. Values are the means of 13 observation periods. Significant differences (P~0.05) between inbred lines are indicated by different letters. CV, coefficient of variation.

LAR than did CS lines. This was associated with a significantly lower SLA, which indicates that dry matter contributed to a lesser extent to the increase in leaf area in CT lines. These lines also tended to allocate more dry matter to the ‘stem’, as indicated by its lower LWR. As with RGR, differences in RLGR can be explained by differences in NAR and LAP. Since CT lines invested a similar amount of newly acquired assimilate into leaf expansion (LAP) compared to CS lines, the greater RLGR of CT lines was due mainly to their significantly greater NAR. In this experiment, therefore, it is clear that the physiological component of growth (NAR) was more important for an efficient dry matter accumulation and leaf area expansion than were the morphological components of growth (LAR, SLA, LAP). Differences in growth strategies are evident when individual inbred lines are compared. Z 15 had the lowest LAR, LAP, and SLA (i.e., ‘thickest’ leaves) but, because of compensation by the highest NAR, RGR and RLGR remained high. Penjalinan had the highest LAR and SLA and a high LAP but, because it had the lowest NAR, it also had the lowest RGR and RLGR. In lines with similar NAR (KW 1074 and CM 109), the higher RGR and RLGR of KW 1074 were the result of its higher LAR, LAP, and SLA. Thus, when comparing indi-

vidual inbred lines, the negative relationships between RGR (and RLGR) and LAR, LAP, and SLA were less clear. Overall, RGR and RLGR were significantly correlated (r = +0X3***), underlining the importance of leaf expansion in the dry matter accumulation of young maize plants. Genetic variability in growth parameters, as represented by the coefficient of variation, was greatest for NAR (Table 3). Since NAR was strongly related to RGR and RLGR, this parameter may prove to be a valuable parameter for selection. Relatively great genetic variability was also found for parameters which are easier to determine, such as the rate of leaf appearance (RLA) and SLA. However, the relationship between those parameters and RGR (and RLGR) was less clear. Because SLA and NAR were negatively correlated (I= -0.57***), SLA may be used as an indirect measure of NAR. 3.2. Growth parameters and environmental conditions To examine the effects of environmental conditions on growth parameters, linear regressions between growth parameters and all measured environmental conditions (Table 1) were compared.

M. J. Verheul et al.lEuropean Journal of Agronomy 5 (I 996) 3 I-43

Data for all lines and all observation periods were used. The results (Table 4) show that temperature was the main factor controlling the growth and development of maize. The strongest correlation coefficient was found for the growth parameter NAR, but RGR, RLGR, NAR, RLA, and RUE were also positively correlated with temperature. The best correlation coefficients were found with mean daily air temperature, with the exception of RUE which showed a closer correlation with minimum air temperature. The growth parameters LAR, SLA, LWR, and LAP were negatively correlated with temperature. Closest correlations for LAR, SLA, and LWR were found for soil temperature. Radiation and amount of rainfall were less important than temperature in determining growth and development. Global radiation apparently determined LAP. The strongest correlations with global radiation and with the amount of rainfall were found with NAR (r= +0.49***) and SLA (r = + 0.42**) respectively. There was no correlation between RUE and global radiation. RUE may, therefore, be a better parameter than NAR when comparing growth responses to temperature in an environment with different levels of global radiation. When growth parameters of individual inbred lines were related to environmental conditions using linear regressions, no interactions between inbred lines and environmental conditions were found (data not shown). The temperature range in the present experiment, with mean daily air temperTable 4 Best correlations (Table 1) Growth

(r) and slopes of best fitted linear regressions

parameter

RGR (g g-’ day-‘) RLGR (m’ m -’ day NAR (g m-’ day-‘) LAR (cm2 g-l) SLA (cm’ g-‘) LWR LAP (cm’ g-‘) RLA (leaves day-‘) RUE (g MJ-’ PAR)

Environmental

‘)

Data for all six lines during ***P~o.oOOl.

condition

Ta,mcan TB,llleP” Ta,lllsa” T,,il Toil

Xi GR T8,lnCBn Cmin autotrophic

growth

in 13 observation

31

atures between 11.0 and 16.6”C, was probably too small for such an interaction to be detectable. CT lines tended to show a larger increase in RGR, RLGR, and NAR with increasing mean daily air temperature than CS lines, but these differences were not significant (data not shown). When growth responses to different sowing dates and elevations were compared, it was found that significant differences existed for growth parameters of maize lines which had been sown early as compared to those of lines sown later (Table 5). Sowing which occurred earlier than usual at a given altitude significantly reduced RGR, RLGR, NAR, and RLA, whereas LAR and LAP increased slightly. Growth parameters of lines sown at a higher elevation generally showed an intermediate response. To evaluate growth responses to different temperature conditions, periods of observation were divided into two groups: mean daily air temperature I 14°C (‘stress’ environments) and mean daily air temperature > 14°C (‘recovery’ environments). The growth parameters RGR, RLGR, NAR, and RLA were significantly lower in stress environments than in recovery environments, whereas LAP was significantly greater in stress environments (Table 5). Thus, the physiological component of dry matter accumulation (NAR) was more sensitive to temperature than were the morphological components (LAR, SLA, LWR). RLGR was less sensitive to temperature than RGR due to a greater investment of newly acquired dry

between

growth

parameters

(Table 3) and environmental

r

Slope

Standard

0.69*** 0.71*** 0.75*** -0.55*** -0.44*** -0.43*** -0.33** 0.66*** 0.64***

0.0140 0.0136 0.895 -0.00137 -0.00119 -0.0138 - 0.00045 0.0233 0.141

0.0017 0.0016 0.091 0.00024 0.00028 0.0033 0.00015 0.0026 0.019

periods

were used (n = 78). Significance

of regressions:

conditions

error of slope

**PI

0.001;

M. J. Verheul et a/./European Journal of Agronomy 5 (1996) 31-43

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Table 5 Growth parameters (Table 3) of young maize plants after early (25 May 1989 and 26 May 1990) and usual (8 June 1989 and 17 June 1990) sowing dates at low altitude (550 m a.s.l.), at a usual sowing date at high altitude (8 June 1989; 720 m a.s.l), and after periods of cold stress (mean daily air temperature between two successive harvests I14”C) and recovery (mean daily air temperature between two successive harvests > 14°C) Parameter

Usual sowing

Early sowing (%)

High elevation (%)

During stress (%)

During recovery (%)

RGR (g g-r day-‘) RLGR (m2 me2 day-‘) NAR (g mm2 day-‘) LAR (cm2 g-r) SLA (cm’ g-‘) LWR LAP (cm2 g-‘) RLA (Ieaves day- ‘) RUE (g MJ - ‘ PAR)

0.139 (a) 0.119 (a) 6.65 (a) 226 (a) 297 (a) 0.759 (a) 189 (a) 0.208 (a) 0.98 (a)

81 (b) 84 (b) 74 (c) 107 (a) 104 (a) 102 (a) 107 (a) gg tb) 75 (b)

89 (ab) 102 (ab) 87 (b) 97 (a) 100 (a) 98 (a) 113 (ab) 95 (ab) 82 (ab)

73 (b) 81 (b) 69 (c) 104 (a) 104 (a) 101 (a) 114 (b) 83 (b) 74 (b)

104 (a) 103 (a) 101 (a) 101 (a) 100 (a) 101 (a) 98 (a) 103 (a) 96 (a)

Absolute values of growth parameters after usual sowing dates at low elevation are shown; other data are expressed as percentages of this value. Significant differences (P10.05) between observation periods are indicated by different letters.

matter into new environments.

leaf area

(LAP)

in

stress

3.3. Plant development Plant development was first analysed in terms of rates of leaf appearance (RLA) based on chronological time (Table 3). However, since temperature strongly influences rates of leaf appearance with chronological time, plant development may be better described by thermal time. From the linear regression of RLA on mean daily air temperature (Table 5), an extrapolated base temperature of 6°C and a thermal duration of 43 degree days were found for RLA. Assuming a base tem~rature of 6°C genotypic va~ability in RLA in thermal time (Table 6) was less than in chronological time (Table 3). On the other hand, when analysed in a thermal time base, CT lines were more clearly distinguishable from CS lines. 3.4. Net photosynthesis Rates of net photosynthesis (PN), measured during the field trial sown early in 1990, varied with environmental conditions and dates of measurement. Significant differences in P, were also observed among inbred lines, as represented by 2 7 and Penjalinan (Table 7). Averaged over dates of measurements, the PN of

Table 6 Rate of leaf appearance (RLA) of young maize plants under field conditions in spring as calculated on a thermal time basis (Tb=6’C)

Inbred line

RLA (1°C day)

KW 1074 Z 15 27 Penjalinan MO 17 CM 109 CT CS Mean cv (%)

0.0244 (ab) 0.0223 (abc) 0.0257 (a) 0.0219 (cd) 0.0189 (d) 0.0239 (ab) 0.0241 (a) 0.0216 (b) 0.0229 10.4

Significant differences (P10.05) between genotypes are indicated by different letters. CT, KW 1074, Z 15, and Z 7. CS, Penjalinan, MO 17, and CM 109. CV, coefficient of variation.

all six inbred lines was highly correlated with the NAR of lines in the same period of observation 0”= “I-0.87**; IZ= 6), underlining the strong relationship between both parameters. Similarly, PN was negatively correlated to SLA (r= -0.97***; n--6). 3.5. Contents of dry matter and carbohydrates

Plant samples of the CT line Z 7 and the CS line Penjalinan were taken at harvests during the

39

M. J. Verheul et al.~Euro~e~ Journal of Agronomy 5 (1996) 31-43

Table 7 Net photosynthesis of the fourth leaf and contents of soluble carbohydrates and starch in the shoots (as percentages of total dry matter) of two maize lines (Z 7 and Penjalinan) during the early sown field trial in 1990 Date

Net photosynthesis (pm01 mm2 s-r) 21

28 May 90 29 May 90 5 June 90 10 June 90 12 June 90 16 June 90 22 June 90

Penjalinan

9.19

6.20

17.51

14.83

17.49

11.96

Soluble carbohydrates (% dm)

Starch (% dm)

Z 7 (SE)

Penjahnan (SE)

Z 7 (SE)

Penjalinan (SE)

5.76 (0.46)

4.50 (0.44)

7.75 (0.55)

5.07 (0.45)

8.67 (0.35)

6.39 (0.36)

4.32 (0.42)

4.08 (0.37)

6.65 (0.36)

4.17 (0.35)

2.92 (0.43)

2.95 (0.36)

1.77 (0.33)

1.57 (0.31)

1.42 (0.39)

1.01 (0.32)

SE, standard error of mean.

early-sown field trial in 1990. No significant differences were found for shoot dry matter contents between lines (10.65 and 10.45% of their fresh weight) or between harvest dates (data not shown). The line Z 7 had significantly greater contents of soluble carbohydrates and starch than Penjalinan (Table 7). The greatest contents of soluble carbohydrates were found in plants harvested after a stress period (5 June 1990) and lowest contents after a recovery period (22 June 1990). The starch content decreased with time in both lines.

4. Discussion The results show that RGR and RLGR are significantly correlated, underlining the importance of leaf expansion for dry matter accumulation of young maize plants, as found by several authors (Milthorpe, 1959; Duncan and Hesketh, 1968; Watts, 1973; Stamp, 1981; Miedema, 1982; Crevecoeur and Ledent, 1984; Hardacre and Turnbull, 1986; Pollock, 1990). Differences in RGR and RLGR among lines during autotrophic growth were mainly due to differences in NAR. The lower LARs of CT lines were contrary to expectations, because a lower LAR reduces potential RGR and RLGR. Poorter and Remkes (1990) attributed the variation in the RGR of 24 wild species to differences in LAR rather than to differences in NAR. Tollenaar (1989) stated that differences in growth rates between maize hybrids were positively related to LAP. The relative importance of NAR and LAR, however, may be dependent on species and

environment (Rajan et al., 1973): the results of Tollenaar (1989) were based on two hybrids only. LAR may be related to other genetic factors rather than to the degree of cold tolerance per se. Hardacre and Eagles (1989) found a lower LAR in a cold tolerant highland tropical hybrid than in corn belt dent hybrids. The low LAR of CT lines under chilling conditions in the field in the present experiments may be of importance in cold tolerance, for a low LAR was significantly associated with a low SLA (r = +0.90***). Because differences in SLA can be ascribed either to morphological factors or to the chemical composition of leaf biomass (Dijkstra, 1989), the lower SLA may be related to a more xeromorphic growth habit, which protects against cold, to a greater amount of photosynthetically active structures per unit leaf area, and/or to a greater carbohydrate content. Chilling-tolerant maize genotypes are known to have thicker leaves due to a thicker mesophyll layer (Thiraporn and Geisler, 1978), a thicker wax layer, and a thicker cuticule. The relation between SLA and the amount of photosynthetically active structures per unit leaf area was indicated by the highly significant negative correlation between SLA and P, found in the early sown field trial in 1990. In the same trial, PN appeared to be related to chlorophyll content rather than to carotenoid content, the activity of ribulose 1,5-biphosphate carboxylase, or to NADP malate dehydrogenase (Picatto, 1992). Akiyama and Takeda (1975) observed a positive relationship between NAR and the rate of photosynthesis in maize. This positive

40

M.J

Verheul et al./European Journal of Agronomy 5 (1996) 31-43

relation between NAR and P, was confirmed in the early sown field trial in 1990. Since SLA and NAR were negatively correlated during all observation periods, the greater NAR observed in CT lines might be due to a greater amount of photosynthetically active structures per unit leaf area. Alberda (1969) showed that low temperatures cause an increase in carbohydrate content in maize plants. This accumulation does not contribute to structural growth (Frossard and Friaud, 1989) but can increase the thickness of the leaf and indicates that growth is inhibited to a greater extent than photosynthesis (Brouwer et al., 1973). Soluble sugars can contribute to an increased rate of leaf growth after a period of stress (Kleinendorst, 1975) and may have a protective effect at chilling temperatures by contributing to the osmotic potential of the cells and by decreasing the oxygen availability for nonmetabolic oxidative reactions which lead to cellular destruction (Purvis, 1990). In the present experiments, a greater concentration of carbohydrates was found in the CT line Z 7 than in the CS line Penjalinan, indicating that Z 7 produced more carbohydrates than it used. Z 7 had a greater RGR and PN than Penjalinan, thus showing that accumulation was due to a greater production of assimilates rather than to a lower consumption of assimilates in growth. Watts (1973) demonstrated that soil temperature is the dominating factor governing leaf area expansion in young maize plants. Under chilling conditions in the present experiment, RGR and RLGR were best related to mean daily air temperature. However, a good correlation between RLGR and soil temperature (r = +0.65***) was also found. Of all parameters, NAR correlated best with temperature (Table 4). LAR and LAP were less closely and even negatively correlated with temperature. The present results are contrary to those of Potter and Jones (1977) and Tollenaar (1989) which were obtained at constant controlled temperatures. Under such conditions, it may be expected that plant growth is more or less in a steady state where LAP equals LAR (Poorter, 1989). In the present experiment, no significant interactions among growth parameters were found between inbred line and temperature. This may have been a consequence of the small temperature range and the fact that all lines were conditioned

to low temperature which can reduce differences in reactions (cf. Stamp, 1984). At near optimal temperature in a growth chamber, it was found that CT lines and CS lines had equal growth potentials (Verheul, 1992; Verheul and Stamp, 1994). Differences in growth reactions to temperature, as found by Potter and Jones (1977), Tollenaar (1989), and Poorter and Remkes (1990), when compared to those found in the present experiment may reflect the fact that the analyses were made for shoot growth only and not for the whole plant. On the other hand, the results presented here were confirmed for whole plants too (Wolfe, 1991). Tollenaar (1989) found a close correlation between RGR of the whole plant and RGR of the shoot under different temperature regimes. At low temperature, the shoot/root ratio in maize was shown to be strongly reduced (Hardacre and Turnbull, 1986) but greater in maize hybrids, which exhibited better tolerance to cold (Hardacre and Eagles, 1989). Thus, according to these authors, shoot dry matter accumulation was more impaired at low temperature than was root dry matter accumulation, especially in cold-sensitive genotypes. From this it is expected that, when based on the whole plant instead of on shoot weight only, the relative difference in LAR between CT lines and CS lines, as found in the present experiment, will decrease. However, Richner’s observations (Richner, 1992) showed that, on average under field conditions in spring, there were no significant differences in the shoot/root ratio of young plants of Penjalinan and Z 7; LAR of 27 was lower than LAR of Penjalinan when calculated for the dry weight both of the shoot and of the whole plant. In the present experiments, effects of light intensity may have modified effects of temperature. Growth parameters, such as NAR, depend strongly on temperature and on global radiation; RUE was, therefore, calculated to account for the effect of radiation on growth efficiency. The highly significant correlation coefficient between RGR and RUE (r= +0.66***) indicated that, when corrected for the effect of radiation, differences in relative growth rates were still related to differences in the efficiency of photosynthetic leaf area to produce dry matter. A careful interpretation is required in comparing

M. J. Verheul et al./European Journal of Agronomy 5 (1996) 31-O

the RUE of different lines, because the RUE is based on several assumptions: the selected value of the extinction coefficient may not be appropriate at low LA1 and may differ among inbred lines, due to differences in light absorption (cf. Kiniry et al., 1989; Gallo et al., 1993). However, since a greater absorbance is expected in CT lines with thicker leaves (e.g., Z 15) as compared to the CS line Penjalinan, which has relatively thin leaves, differences in RUE may even increase when absorption is taken into account. In the present experiment, relatively low values were obtained for RUE compared to values of around 3 g MJJ’ which are generally found for maize (Tollenaar and Bruulsema, 1988; Kiniry et al., 1989). RUE values around 3 g MJJ’ were, however, obtained on average between emergence and anthesis in maize crops grown at temperatures between 19 and 26°C. Careful interpretation is needed, because RUE values may differ as a result of the methodology used (cf. Gallo et al., 1993). Andrade et al. (1993) found that low temperature (15-18°C) during the vegetative growth phase reduced the RUE of maize. The positive association between RUE and temperature in maize, over mean temperatures between 15.8 and 20.9”C, as reported by Andrade et al. (1993), was confirmed in the present experiment for mean temperatures between 11.0 and 16.6”C (Table 1 and Table 4). Schapendonk et al. (1994) related low values of RUE to the sensitivity of maize to photoinhibition. In the present experiments, RUE showed the closest correlation to minimum air temperature; photoinhibition is also more severe at lower temperatures (Long, 1983). Moreover, it was observed that photoinhibitory reductions in photosynthesis in maize increase when low temperatures coincide with high light intensity in a controlled environment (Long et al., 1983) and in the field (Farage and Long, 1987; Long et al., 1994). Analysis of plant development is often based on thermal time, because temperature strongly influences rates of leaf appearance over chronological time (Ong and Baker, 1985). In the present experiment, best fits were found when mean daily air temperatures were accumulated, above a base temperature (7”) of 6°C. CT lines tended to have a lower Tb than CS lines (5.1 and 7.O”C,respectively).

41

For maize grown under northern European conditions, Carr and Hough (1978) and Durr et al. (1991) suggested base temperatures between 6 and 8°C. Thermal duration, the length of time for a new leaf to develop, was approximately 43 degree days in the present experiment. This was in agreement with the results of Picard et al. (1985) in field studies; they reported a thermal duration of 35-43 degree days with a base temperature of 6°C. At temperatures below 16°C thermal duration may increase considerably, as shown in growth room studies by Warrington and Kanemasu (1983).

5. Conclusions The results of this study provide clear evidence that, during early autotrophic growth of maize under chilling conditions in the field, a more efficient shoot dry matter accumulation and leaf area expansion is related to a greater photosynthetic capacity per unit leaf area rather than to a favourable leaf morphology or a better use of assimilates. Considerable variability between groups of lines was found for NAR, which suggests the possibility of success in breeding for improved cold tolerance. Since NAR and PN were negatively correlated with SLA, which is easy to determine, SLA may be used to select indirectly for NAR and P,.

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