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Crop Science 43:874-878 (2003)
© 2003 Crop Science Society of America

CROP PHYSIOLOGY & METABOLISM

Base Temperatures for Seedling Growth and Their Correlation with Chilling Sensitivity for Warm-Season Grasses

I. C. Madakadzea, K. A. Stewartb, R. M. Madakadzea and D. L. Smith*,b

a R.M. Madakadze, Dep. of Crop Science, Univ. of Zimbabwe, P.O. Box MP 167, Mount Pleasant, Harare, Zimbabwe
b Dep. of Plant Science, McGill Univ., 21-111 Lakeshore Road, Ste-Anne-de-Bellevue, QC, Canada H9X 3V9

* Corresponding author (dsmith{at}macdonald.mcgill.ca)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Initial screening of warm-season grasses for cultivation in cool, short season growing areas has been focused on frost and chilling tolerance. Adoption of warm-season grasses in these areas has resulted in an increase in degree-day modeling of their growth. These predictive models are dependent on accurate determination of the basal temperatures for growth. In this study, base temperatures for seedling growth were estimated for switchgrass (Panicum virgatum L.), big bluestem (Andropogon gerardii Vitman), Indian grass (Sorghastrum nutans L. Nash), and prairie sandreed [Calamovilfa longifolia (Hook) Scribn.]. Seedlings at the two-leaf stage were grown at 4, 8, 12, 16, and 24°C in growth chambers for 4 wk with representative harvests every week. Relative growth rates were calculated for each species at each temperature and these were used, in conjunction with regression techniques, to estimate base temperatures for growth. The base temperatures were then correlated with chilling sensitivity of the plants, estimated using visual scores, chlorophyll fluorescence, and electrolyte leakage. The estimated base temperatures ranged from 2.6 to 7.3°C. There were variations among and within species in base temperatures for seedling growth. There were positive correlations between base temperatures for growth and rate of electrolyte leakage (r = 0.73), chlorophyll fluorescence (FV/FM; r = 0.80) and leaf damage (visual score; r = 0.76). These correlations confirm the differences in adaptation of warm-season grasses, both within and across species. They also support the differences in base temperatures. This highlights the need to use different base temperatures in statistical growth models for different species or cultivars.

Abbreviations: CIR, ‘Cave-in-Rock’ • FV, variable fluorescence • FM, maximal fluorescence • RGR, relative growth rate • Tb, base temperature


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
THE WIDESPREAD ADOPTION of warm-season grasses in cool, short-growing-season areas has led to the development of heat-unit-based models of the effects of temperature on their growth (Lawlor et al., 1990; Probert, 1992; Unruh et al., 1996). Slow stand establishment under low temperatures is of particular interest. Postemergence slow stand establishment may be caused by slow seedling growth and late development of the root system (Unruh et al.,1996). Relationships between growing degree-days and rates of morphological development have been used to schedule management of warm-season grasses (Mullahey et al. 1990, 1991; Sanderson and Wolf, 1995a). Sanderson and Wolf (1995b) also used growing degree-days to study seasonal changes in the chemical composition of switchgrass. However, the models used by these authors are dependent on accurate determination of the minimum or base temperature (Tb) for the particular growth phase. Several studies, including Mullahey et al. (1990), Sanderson and Wolf (1995b), Mitchell et al. (1997), and Sanderson and Moore (1999), have included development of growth and management models. However, these models utilized blanket base temperatures for many cultivars and across all growth stages. For pearl millet {Pennisetum typhoides (Burm. f.) Stapf & C.E. Hubb. [= P. glaucum (L.) R. Br.] (Ong, 1983)} and groundnut [Arachis hypogaea L. (Leong and Ong, 1983)], there were only small variations in Tb for different growth and developmental phases. However, for wheat (Triticum aestivum L.), values of Tb have been reported to vary depending on plant age (Angus et al., 1981) and phenological stage (Slafer and Savin, 1991).

Warm-season plant growth at suboptimal temperatures can also be explained in terms of chilling tolerance. The term chilling injury describes the visual manifestation of the cellular dysfunction that occurs in plants when exposed to chilling temperatures (0–20°C) (Raison and Orr, 1987). In the cool, short growing areas, this occurs in spring and fall. A great deal of research has been conducted to assess chilling tolerance or injury using various techniques such as electrolyte leakage, protoplasmic streaming (Graham and Patterson, 1982) and chlorophyll fluorescence (Hetherington et al, 1989). Some of the warm-season grass species have evolved tolerance to chilling temperatures (Lee and Estes, 1982; Stamp et al., 1983). Conceivably, the ecophysiological pressures exerted on the species or cultivars have affected the respective degree of chilling tolerance attained. These pressures would have occurred during cultivar development or subsequent repeated production in a given geographical area. Differences in chilling tolerance could, therefore, be largely due to different areas of origin (Jacobson et al., 1986; Sthapit et al, 1995). As a result, Tbs for growth, for example, would be related to the chilling tolerance of the species or ecotype. This study was therefore conducted to (i) determine the Tbs for growth of cultivars of switchgrass, big bluestem, Indian grass, and prairie sandreed, and (ii) validate the Tb values by evaluating their correlation with chilling sensitivity.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The study was conducted using four switchgrass cultivars: ‘Cave-in-Rock’ (CIR, originally developed from southern Illinois), ‘Dakota’ (from North Dakota), ‘Pathfinder’ (from Nebraska), and ‘New Jersey 50’ (NJ50, from North Carolina); two big bluestem cultivars ‘Bison’ (from Nebraska), and ‘Niagara’ (from NW New York); two Indian grass cultivars ‘Holt’ (from Nebraska) and ‘Tomahawk’ (composite from North and South Dakota) and two prairie sandreed cultivars ‘ND95’ (from North Dakota) and ‘Pronghorn’ (from southern Nebraska).

Base Temperature for Seedling Growth
Ten to 15 seeds of each entry were initially sown in 12.5-cm diameter pots containing 2:1:1 (v/v/v) promix (Premier Horticulture Inc., Riviere-du-Loup, QC, Canada), vermiculite (Vil Vermiculite Inc., Montreal) and free draining St. Bernard loam (Hapludalf soil) obtained from the Emile Lods Research Centre of McGill University. The seeds were allowed to germinate in a greenhouse maintained at 24°C and under natural light conditions with supplementary automatic lighting to maintain a 14-h daylength and at least 400 µmol m-2 s-1 PAR as measured with a Li-19SA Line Quantum Sensor (Li-Cor Inc., Lincoln, NE, USA). The seedlings were watered as necessary and fertilized as per recommendation (0.33 g L-1) with water soluble 20-20-20 NPK mix (Plant Products Co. Ltd., Brampton, ON, Canada). The fertilizer was applied as a water solution once a week. At the two-leaf stage, the pots were thinned to five comparable plants per pot. On the basis of prior experience, the different cultivars were germinated at different times to synchronize the beginning of the experiment, so that all seedlings would be at the same full two leaf growth stage at the start of the work. The pots were then transferred to growth chambers (Conviron ModE15, Controlled Environments Ltd., Winnipeg, MB, Canada) that were randomly assigned to constant temperatures of 4, 8, 12, 16, and 24°C. Four pots of each cultivar were randomly placed in each chamber. At the end of each of four consecutive weeks, one pot per cultivar was removed and the plants were washed free of the potting mixture, dried for 48 h at 80°C and weighed for total biomass determination. Plants that were comparable to those remaining in the pots after from the thinning exercise were used to estimate total biomass at the beginning of each replication of the entire experiment. The experiment was a five (temperature) by 10 (cultivar) by four (harvest time) factorial experiment organized following a completely randomized design with three replications across time.

Biomass changes across the four harvests were subjected to linear regression analysis and the slope of each of the fitted lines provided an estimate of mean relative growth rate (RGR) during the four weeks (Poorter and Garnier, 1996). The changes in RGR with temperature for each cultivar were subjected to nonlinear regression analysis using either of two equations. The first equation (Eq. [1]) was of the form

[1]
where 1/t represented RGR; T, growth temperature, Tb is the base temperature at which 1/t = 0; and k is a constant (Garcia-Huidoboro et al., 1982). The condition that T > Tb otherwise 1/t = 0, was also mandated in the analysis. The second equation (Eq. [2]) was an exponential relationship of the form

[2]
where k is a growth rate constant (Unruh et al., 1996).

Chilling Sensitivity
Chlorophyll Fluorescence and Visual Assessment
Chlorophyll fluorescence [(FV/FM), variable fluorescence divided by maximal fluorescence] of four-leaf stage plants produced at 24°C in a greenhouse as for the base temperature study was measured using the Morgan CF-100 Chlorophyll Fluorescence System (Morgan Scientific Inc., MA, USA). The plants were then placed for 4 d in growth chambers maintained at 4°C and 14-h daylight at 400 µmol m-2 s-1. After 4 d at chilling temperatures, the plants were transferred to a greenhouse kept at 24°C and full sunlight in early autumn (supplemented with artificial light to maintain a 14-h daylight regime). Decline in chlorophyll fluorescence (FV/FM), measured 4 d after transfer to the greenhouse (recovery period), was expressed as a percentage of the pre-chilling values. The experimental design was a completely randomized design and 16 plants per cultivar were used as replications.

The same plants were also assessed visually for chilling injury during the recovery period. The symptoms evaluated included wilting and browning, chlorosis and/or changes in leaf color. The intensity of the visual symptoms was scored on a scale of 0 to 5 (none visible to severe damage) and proportion of leaf area affected was also scored as a percentage of total leaf area (Cappell and Doerffling, 1993).

Electrolyte Leakage
Seedlings were produced as for the base temperature study and allowed to grow to four or five expanded leaves. For each cultivar, eight replicate 50-mL capped bottles containing 10 leaf discs of 0.8-cm diameter in 10 mL deionized water were used. The discs were taken midmorning before the beginning of each repetition using a metal disc punch. The capped bottles were placed on ice in a covered cooler box (to ensure darkness). The conductivity of the deionized water holding the 10 leaf discs was measured daily, including an initial measurement before placement on ice, using a conductivity meter, as adopted from the technique of MacRae et al. (1986). At the end of 22 d, total ion content of each sample was determined by boiling in 10 mL of deionized water for 2 min, cooling to room temperature, and measuring conductivity. The daily conductivity readings were expressed as a percentage of the total. The rate of electrolyte leakage was computed as the regression coefficient of conductivity across time. The experiment was organized following a completely randomized design with eight replications, with repeated daily measurements for 22 d. This experiment was repeated three times.

Statistical Analysis
The regression analysis and ANOVA for the base temperatures were performed using SAS procedures (SAS Institute, 1996). Simple correlation analysis was performed between cultivar mean data for the chilling sensitivity variables and base temperature, again using SAS procedures.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS
 REFERENCES
 
Seedling Growth
As growth temperature increased, total dry matter increased for all cultivars (examples in Fig. 1). These dry matter increases were similar to those reported by Hsu et al. (1985). Relative growth rate values were obtained by linear regression using natural-log-transformed dry matter weights. The cultivar x temperature interaction was significant (P < 0.05) across the temperature range studied. The increases in RGR with temperature were linear in Bison, Dakota, ND95, and Pronghorn, and exponential for the rest of the cultivars studied (Fig. 2). Estimations of Tb and growth constants were made using nonlinear regression analysis with either Eq. [1] or [2], depending on the relationship (Fig. 2).



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  		Fig. 1. Total dry weight changes with time for ‘Cave-in-Rock’, ‘Holt’, ‘Pronghorn’, and ‘Niagara’ seedlings under different temperatures. Different scales on the y-axes are indicative of the relative sizes of the seedlings from the different species. Error bars denote standard error.

 


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  		Fig. 2. The effect of temperature on the relative growth rates of warm-season grass seedlings. Error bars denote standard error.

 
The highest Tb was estimated for CIR, followed by NJ50 and Niagara (Table 1) and the lowest was for Bison. Among the switchgrasses, the ranking in Tb for growth was, in increasing order, Dakota, Pathfinder, NJ50, and CIR. Niagara big bluestem had a higher Tb value than Bison. There was no difference between the two Indian grasses or between the two prairie sandreed cultivars. The growth rate constants did not follow the same ranking as the Tb values. Cave-in-Rock had a higher growth rate constant than all the other cultivars tested. Different ranking in growth rate constants might have been due to the use of total dry weight. Hsu et al. (1985) reported higher growth rates for aboveground tissues than roots.


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  		Table 1. Estimations of the base temperatures (Tb) and growth constants (k) for seedling growth of warm-season grasses.

 
The Tb values for growth seemed to confirm the low spring growth observed in the field for CIR and NJ50, and the early spring growth by Dakota, Pathfinder, and the prairie sandreed cultivars (Madakadze et al., 1998). Given differences in places of origin, at least for the switchgrasses and big bluestems tested, differences in Tb for growth might also be due to differences in evolution patterns of these cultivars, or at least the parent populations. As was noted for common centipedegrass [Eremochloa ophiuroides (Munro) Hack.] (Unruh et al., 1996), the slow spring growths of CIR and NJ50 were followed by rapid growth as the temperatures increased. In a field evaluation (Madakadze et al., 1998), these two cultivars were the highest yielders. However, only moderate yields were recorded for Pathfinder, which in this study had a combination of a relatively low Tb for growth and a high growth rate constant.

Chilling Sensitivity
Other than for Tomahawk and Bison, no visual injury to the evaluated cultivars was evident during exposure to 4°C. Both Tomahawk and Bison showed purpling and partial wilting of some leaves. On returning the plants to warm temperatures, various visual symptoms of chilling injury were evident. These ranged from leaf chlorosis (yellowing and purpling), browning/necrosis, to wilting. The ranking of the cultivars based on leaf area damaged, in increasing order of sensitivity (P < 0.05), was Tomahawk (30%) < ND95 (36.5%), Pronghorn (38.5%), Dakota (40.4%) < Pathfinder, Holt (40.8%), Bison (42.5%) < Niagara (46%) < NJ50 (53%) < CIR (56%).

Differences in electrolyte leakage were not discernible after 48 h so that ranking of the entries was not possible. However, there were increases in ion leakage at 22 d. Relative rate of electrolyte leakage, and not total leakage, was the preferred measure of chilling sensitivity because differences in leaf fresh weight and structure have the potential to affect absolute leakage values. The ranking for rate of leakage (% leakage d-1), in increasing order (P < 0.05), was Dakota (0.086) < Tomahawk (0.096) < Bison (0.116) < Holt (0.129), NJ50 (0.131) < Niagara (0.147), ND95 (0.145) < Pronghorn (0.158) < CIR, Pathfinder (0.164). This ranking was not the same as that based on visual assessment.

Chlorophyll fluorescence measurements showed a differential loss in photosystem activity among the entries. The decline in FV/FM ranged from 6.6 to 32.5%. These values were low, given that the plants were allowed 4 d of recovery at 24°C following photoinhibitory chilling. The ranking of the cultivars (P < 0.05), Bison (6.6%), Tomahawk (7.9%) < ND95 (11.4%) < Pronghorn (16.9%) < Dakota (19.3%), Holt (19.6%) < NJ50 (25.4%) < Niagara (27.9%) < Pathfinder (30.9%), CIR (32.5%), was closer to that of the visual assessment than the one based on electrolyte leakage. The decline in FV/FM was higher for more chilling sensitive entries, indicating a greater sensitivity (r = 0.8 as shown in Fig. 3) of these cultivars to photoinhibition. Similar changes in FV/FM have been reported previously for several plant species (Hetherington et al., 1989; Verheul et al., 1995).



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  		Fig. 3. The correlation of (A) chlorophyll fluorescence, (B) leaf damage, and (C) rate of electrolyte leakage with base temperature for seedling growth in warm-season grass seedlings subjected to cold stress. Error bars denote standard error.

 
The chilling sensitivity (as based on electrolyte leakage, chlorophyll fluorescence, and leaf damage symptoms discussed above) of the cultivars and ecotypes correlated well with the determined base temperatures for seedling growth (Fig. 3). The correlation was highest with FV/FM, the simpler and probably more objective assessment of chilling tolerance. These strong correlations highlight the differences in adaptation of warm-season grasses, both within and across species. There is, therefore, a need to use different base temperatures for different species and ecotypes, and these were corroborated by chilling sensitivities. Adoption of different base temperatures can only improve the predictive growth equations reported by Sanderson and Wolf (1995b), Mitchell et al. (1997), and Sanderson and Moore (1999). It is also conceivable, as in maize (Stewart et al., 1998; Dwyer et al., 1999), that there are different thermal functions for different growth stages. These different stages might require different base temperatures. Therefore, the use of one base temperature for all growth stages could be fraught with problems. This is further compounded by differences in daylengths of regions of production (Sanderson and Moore, 1999).


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
REFERENCES
 
Intra- and interspecific variations exist in base temperatures for growth in warm-season grasses. This variation probably reflects different places of origin or at least adaptation to specific environmental pressures. Chilling sensitivity of various warm-season grasses correlated well with the determined base temperatures for seedling growth. While this confirms a pattern for base temperatures for growth observed in the field, it also highlights the need to use different base temperatures in statistical growth models for different species or cultivars.


   ACKNOWLEDGMENTS
 
We thank M. Pikarnegar, R. Smith, and S. Liebovitch for their technical assistance.

Received for publication January 7, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 




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