Assumptions of Plastochron Index: Evaluation With Soya Bean Under Field Drought Conditions
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1 Am. Bot. 50, , 1982 Assumptions of Plastochron Index: Evaluation With Soya Bean Under Field Drought Conditions J. S. VENDELAND, T. R. SINCLAIR*, S. C. SPAETH* and P. M. CORTES Microclimate Project, USDA-ARS, Agronomy Dept., Cornell University, Ithaca, New York, U.S.A. Accepted: 23 March 1982 ABSTRACT Erickson and Michelini (1957) derived the plastochron index (PI) and a term sometimes referred to as the plastochron ratio (PR), as quantitative expressions of the vegetative development of plants. With the stable plant growth in environmental chambers and glasshouses, the assumptions used to derive these terms have been validated. However, more recently these expressions are being used to characterize growth under the unstable conditions resulting from the imposition of stress. This study examines the validity of the assumptions used to derive PI and PR forfield-grownsoya beans [Glycine max (L.) Merrill] subjected to drought stress. Under stress conditions, the assumptions were not satisfied. In fact, observing change in PR appeared to be a good method for detecting drought stress in these plants. An alternate method for calculating PI based on a single, young leaf was developed. This alternate method appeared to be a more sensitive indicator of changes in leaf emergence rate under unstable conditions. Key words: Plastochron index, plastochron ratio, Glycine max (L.), soya bean, drought, leaf growth. INTRODUCTION Watson and Baptiste (1938) reported the results of experiments with field-grown mangolds and sugar beets [Beta vulgaris (L.)] designed to compare destructive and non-destructive techniques for characterizing growth rate. An important non-destructive measurement was simply a count of all leaves over 2-5 cm long. They concluded that the non-destructive sampling provided ' a more accurate estimate of the time changes than the sampled plants, as they were not subjected to plant-to-plant variation'. Furthermore, a measurement technique relying on leaf expansion data has obvious appeal for studying plants in the field because of its potential sensitivity to changing environmental conditions. Leaf initiation and expansion are among the most environmentally sensitive growth processes. Both low temperatures (Watson and Baptiste, 1938; Hesketh, Myhre and Wiley, 1973; Thomas and Raper, 1976) and drought stress (Gates, 1968; Husain and Aspinall, 1970; Clough and Milthorpe, 1975; Marc and Palmer, 1976) reduce the rate of leaf initiation. Water stress can also profoundly affect the rate of leaf expansion (Boyer, 1968; Acevedo, Hsiao and Henderson, 1971; Wenkert, Lemon and Sinclair, 1978). Lamoreaux, Chaney and Brown (1978) reviewed a number of studies that utilize leaf development data to characterize plant growth. The potential for using leaf observations to study growth was greatly enhanced by the development of the plastochron index (PI) by Erickson and Michelini (1957). They developed a method for adding a decimal fraction to the leaf count, allowing much greater resolution in the determination of leaf emergence and growth. The PI of Erickson and Michelini was based on the observation that during the early phases of leaf expansion of Xanthium, growth is nearly exponential, and therefore the logarithm of leaf length in * Present address: Agronomy Physiology Laboratory, University of Florida, Gainesville, Florida 32611, U.S.A /82/ $03.00/0 '982 Annals of Botany Company
2 674 Vendeland et al. The Plastochron Index in Soya Bean this phase of growth is linear with time. Also, under experimental conditions used by Erickson and Michelini, the leaves appeared at a uniform rate and expanded in a similar manner with time. When the lengths of successive leaves are expressed logarithmically and plotted against time, their early expansion phases generate a series of parallel, equally spaced lines (Fig. 1). Because of this regular pattern of lines, Erickson and Michelini chose to use a geometric approach to the derivation of their interpolation. It is important to note the explicit assumptions of their derived PI; for successive leaves' the early portions of the logarithmic growth curve are (1) linear, (2) parallel, and (3) equally spaced'. The derived definition of PI was: log(l B )-log(*) "log(l n )-log(l n+1 )' 0) where n = number of leaves longer than reference length (R), L n = length of leaf n (which by definition is greater than or equal to R) and L n+1 = length of leaf n+1 (which by definition is less than R). A consequence of this derivation is that the denominator of Eqn (1) is assumed to be constant. Erickson and Michelini defined the denominator as the ' relative plastochron rate,' while Horie et al. (1979) called this term the 'relative length growth rate on basis of plastochron'. Most recently, Silk (1980) simply called this logarithm of the ratio of leaf lengths the 'plastochron ratio'. Since we make direct comparisons with the data of Silk, we have used her terminology of plastochron ratio, PR. PR = log- (2) The validity of the assumptions used to derive Eqns (1) and (2) were carefully tested for greenhouse-grown soya beans by Hanada and Yong Son (1974). While they found deviations from the theoretical growth curves as presented in Fig. 1, these caused insignificant errors from a practical standpoint (maximum calculated error was 009 PI). They concluded the assumptions of the PI derivation were valid in practical terms. However, the research of Hanada and Yong Son and many others was done under the relatively stable conditions of a greenhouse or growth chamber. An important question concerns the validity of these assumptions underfieldconditions, particularly when stress is imposed. It seems possible that there may be a differential sensitivity to a stress between leaf n + 1 and n because these leaves will vary in the extent to which cell division and/or Slope. a /jalni. Measuring date n + 2 B /C, Reference / length / Date FIG. 1. Idealized representation of the logarithm of leaf lengths plotted against dates.
3 Vendeland et al. The Plastochron Index in Soya Bean 675 expansion is taking place. Yet Lamoreaux, Chaney and Brown (1978) and Silk (1980) suggested that PI and PR be used to assess the effects of environmental stress on plant development. Clearly, the assumptions underlying this approach must be re-evaluated under these stress conditions. As a partial test of the assumptions under drought, Silk (1980) examined the stability of PR in cantaloupe [Cucumis melo (L.)]. She found the seasonal mean of PR of the irrigated treatment was and in the drought treatment was Since the PR values were essentially identical, she concluded PR did not change in response to water stress. However, this conclusion is worrying because it was based on a comparison of seasonal means of PR that had large standard deviations. Such large standard deviations, themselves, suggest PR was not rigidly constant as assumed in the PI derivation. This study was undertaken to reconsider the assumptions of the PI derivation under field drought conditions. Seasonal changes in PR of soya beans were determined for plants subjected to various periods of drought. Further, an alternate method for determining PI is discussed as an approach to reflect more accurately the responses to stress. METHODS Soya beans [Glycine max (L.) Merrill cv. Wilkin] were sown on 14 May 1979 on Tailby Field in Varna, New York. The cultivar Wilkin (maturity group O) was selected because of its relatively under-developed tap root system and its apparent susceptibility to drought stress. The soil of this site was a gravelly loam having been classified to include Red Hook gravelly silt loam, Dunkirk silt loam and Braceville gravelly loam. Commercial fertilizer of a (N-P 2 O 5 -K 2 O) formulation was broadcast at a rate of 200 kg ha" 1 and harrowed into the soil before seeding. In addition, the seeds were inoculated with Rhizobium japonicum before seeding. Rows were roughly in the north-east-south-west direction and spaced at a distance of 76 cm. After emergence, seedlings were thinned to a spacing of one plant every 3 cm. Weed control was achieved with a pre-emergence treatment of 2 kg ha" 1 of Lasso (Alachlor) and 0-4 kg ha" 1 active Sencor (Metribuzen). Two rain shelters were used so that rainfall could be withheld from two large plots at any one time during the season. These shelters moved on tracks, allowing them to be placed over the water stressed plots during periods of rain, and then withdrawn so as not to interfere with the incident radiation of the crop. Each shelter measured 11 by 8 m and covered one entire treatment. Five treatments, as described in detail in Table 1, were established to impose stress at different stages of growth: 1, vegetative; 2, flowering; 3, seed set; 4, seed fill and 5, unstressed. No deviation in leaf emergence rate attributable to reproductive development was detected until pods developed at the top nodes of the plants (approximately Julian date 205). Therefore, for purposes of this study on vegetative growth, treatments 1, 2 and 3 provided the data for the variability of leaf growth in response to drought. The development of the plants in the various treatments was monitored non-destructively on individuals by repeated measurements of morphological characteristics. At each observation, the length and width of all three leaflets of all trifoliates, petiole length and thickness, internode length, stem thickness, and leaf thickness were measured. For the analysis of the PI concept, the length of the terminal leaflet was used since it was found to correlate very well with leaflet width, leaflet area, and leaf area (Vendeland, 1981). Thirteen plants in treatment 5, 13 in 1, 12 in 2, and six plants each in treatments 3 and 4 were selected at the unifoliolate stage and measured through to the end of seed development. The 50 plants were selected when the unifoliolates were expanded approximately 50 per cent. On each measuring date, all terminal leaflets longer than
4 676 Vendeland et al. The Plastochron Index in Soya Bean TABLE 1. Description of drought treatments on Wilkin soya bean at Varna, New York in Julian dates are in parentheses Treatment number Initiated Stress Terminated Developmental stage during stress 1 14 May 9 July (134) (190) 2 14 June 20 July (165) (201) 3 9 July 6 Aug (190) (218) 4 23 July Harvest (204) 5 None None * Letter and number notation of Fehr et al. (1971). Early vegetative (germination to V5 & Rl*) Late vegetative through to flowering (V2-R2) Flowering through to Seed set (R2-R5) Seed growth (R2-R8) 3-5 mm on a plant were measured with a clear plastic rule. Plants were not measured on a fixed schedule, as weather and field conditions would not allow this. Instead, measurements were constantly being made through the season, rotating through the 50 plants as time and conditions permitted. The range in time intervals was 2-3 days early in the season and 7-10 days at the end of the season. As the plants became larger, the time required to measure each individual increased greatly, resulting in longer intervals at the end of the season. During the imposition or relief of drought, the period of measurements was never greater than 6 days. The time intervals between measurements were generally less than the length of a plastochron. RESULTS Leaflet length data on the stressed soya beans failed consistently to meet the assumptions of Erickson and Michelini's definition of PI. This is illustrated in Fig. 2(a), where the logarithmic leaf length of each leaf on a plant in treatment 2 is plotted against date. It Julian date FIG. 2. (a) Logarithm of leaf lengths plotted against Julian date for plant 37 subjected to drought treatment 2. (b) Plastochron ratio for same plant plotted against Julian date.
5 Vendeland et al. The Plastochron Index in Soya Bean Julian date FIG. 3. Seasonal plot of plastochron ratio for plants subjected to (a) unstressed treatment 5 and to (b) drought treatment 2. Numerals are given where superimposed data occur. is especially clear that, as stress was imposed, the lines for the individual leaves were neither parallel nor equally spaced. In Fig. 2(b), the PR for each of the observation dates is plotted for this same plant, assuming a 15 mm reference length. The 15 mm reference length was chosen after surveying the data because generally the leaves with lengths on both sides of this reference length were in the exponential growth phase. The PR increased substantially upon the imposition of the drought mainly reflecting the differential growth rate between leaves 4 and 5 during the most severe stress. The growth of the smaller, younger leaf was retarded much more than the older leaf when stress was imposed. Clearly, to calculate PI from Eqn (1) for this plant during water stress would violate the assumptions of its derivation. Further, the PI estimate from Eqn (1) would tend to mask the stress response because it is an interpolation between two leaves with differential growth responses. The PR for all plants in treatment 2 are plotted in Fig. 3. For comparison, PR for plants of the unstressed treatment are also plotted in Fig. 3. In both cases, the PR appeared to decrease slightly over the first 10 days of observation (days ). In the unstressed treatment, the PR then remained relatively constant throughout most of the remaining vegetative period. Only the PR data from day 204 show a slight increase, < < 0-25 _ A /\ 7 \ \» \ \ / V, o \ m \ 0-05 O * *% 160 i 170 i 180 i 190 i Julian date FIG. 4. Seasonal plot of leaf emergence rate (API/Af) calculated by single leaf ( methods ( ) for plant 37 subjected to drought treatment 2. ) and two leaf
6 678 Vendeland et al. The Plastochron Index in Soya Bean TABLE 2. Plastochron ratios (±standard deviation) of Wilkin soya bean calculated for the five drought treatments for various periods during the 1979 season Julian dates Treatment All vegetative number stages ± ± ± ± ± ± O-46± ± ±0-19 reflecting the decline in leaf emergence rate associated with the development of pods at the top nodes of the plants. On the other hand, the PR in treatment 2 increased earlier and to a greater extent in response to drought. In contrast to a comparison of seasonal means presented by Silk (1980), these data clearly showed a change in PR through the season in response to water stress. To further illustrate the sensitivity of PR to drought, the mean PR values for each treatment during two intervals in vegetative growth and for the entire period of vegetative growth are presented in Table 2. Little decrease in soil water potential was observed during the period from Julian dates for any of the treatments. Consequently, they had very comparable PR and low standard deviations. However, for the period from Julian dates , both treatments 2 and 3 were subjected to stress and the PR values were substantially increased. The mean PR data for the entire vegetative stages obscure the differences among treatments in PR. The standard deviations of the entire season were also substantially greater for these data. Curiously, the overall mean for each treatment was quite comparable to the PR values reported by Silk (1980). Furthermore, had seasonal changes in PR not been studied it would have been possible to concur with her conclusion that PR is little altered by drought. But temporal grouping of data clearly show this was not the case and contradict the assumptions in the derivation of the PI. DISCUSSION From the data on water stressed soya beans we conclude the PR cannot be assumed to be constant under drought. In fact, it was found that an increase in PR was a good index of drought stress in Wilkin soya bean. The reason PR changed was due to the differential response of the n and n+1 leaves to drought stress. Since the calibration of PI relies on an interpolation between leaves with dissimilar responses, the resultant PI will not accurately reflect the response of either leaf. The sensitivity of PI as an indicator of stress is especially diminished by use of the older, less responsive leaf in Eqn (1). Variation in PR in response to stress posed a second problem for the calculation of PI. The difficulty, of course, is that these data clearly violated the assumptions of the derivation of PI. To further illustrate this problem, Eqn (1) can be rewritten to contain the term PR explicitly. That is, Erickson and Michelini (1957) assumed the value of PR in this expression was constant. If it were not constant, then the decimal portion of the calculated PI would not be accurate.
7 Vendeland et al. The Plastoohron Index in Soya Bean 679 Nevertheless, the above objections may not be too serious in simple characterizations of plant age. They only introduce an error in the decimal fraction of PI. Over relatively long periods of growth these errors will not seriously misrepresent the growth pattern of the plants. On the other hand, calculation of leaf plastochron age or leaf emergence rate over short time intervals when stress is being imposed can result in more serious errors because the decimal fraction becomes a more significant component. To focus more directly on the growth responses of the young leaf, we have used a variation of Eqn (3) to calculate PI from length data for the n + 1 leaf solely. This was done by attempting to assess only the growth of the n +1 leaf in comparison with an ' unstressed' leaf. Therefore, PR was set equal to a constant value observed for unstressed leaves (i.e. PR = 0-43). Further, to allow the n+l leaf to be studied a new, smaller reference length, R', was defined. Therefore, Eqn (3) can be rewritten as pi w + (4) PR Consequently, to make the single leaf calculations of PI the rigorous assumptions of the derivation of Erickson and Michelini do not have to be met. Instead, Eqn (4) assumes first, that all young leaves do or potentially can grow at the exponential rate of an unstressed leaf and secondly, it assumes that the PR of unstressed leaves provides a suitable standard against which to compare the growth of young leaves. Equation (4) then reflects the progress of the n+ 1 leaf with respect to the assumed exponential growth model. The calculations of PI based solely on leaf n +1 rather than on leaves n +1 and n should be essentially identical under stable growing conditions but may differ substantially during unstable conditions. A direct comparison of PI calculated by the Erickson and Michelini method represented in Eqn (1) and by the single leaf formulation of (4) is possible if a value of R' is selected that is comparable to R being defined at 15 mm. In fact, for unstressed leaves the definition of PR can be used to determine R' (i.e. PR = log [R/R']). For PR = 0-43 and R = 15 mm, a compatible R' for comparison of the two methods would be 5-6 mm. Since leaf lengths were measured only to the nearest millimetre, we rounded R' to 6 mm for this comparison. All L n+l were taken to be at least 6 mm long (i.e. 6 mm ^L n+l < 15 mm), so that the decimal fraction was held at 0 until L n+l reached a length of 6 mm. The leaf length data of the plant in Fig. 2(a) were used to calculate PI by both (1) and (4). The PI values calculated by the two approaches never differed by more than 0-36, confirming the essential equality in determining plant age by the two methods. However, there were more significant differences when leaf emergence rates were calculated as API/A/. These results, presented in Fig. 4, show that the single leaf formulation results in a much more responsive index both to the imposition of drought and to the recovery upon irrigation. This, of course, is a result of the greater sensitivity of small, young leaves to changes in stress. Consequently, we have concluded the general concepts of PI and PR are very useful ones to characterize soya bean growth under drought conditions in the field. However, it was discovered that the assumptions in the PI derivation presented by Erickson and Michelini (1957) were violated under these conditions. In fact, monitoring the failure to have a constant PR actually appeared potentially to be a good technique for detecting an early response to drought. An alternate method we developed for calculating PI focuses on the growth of a single, young leaf. It depends less on the original assumptions in the PI derivation because it only assumes a young leaf has the potential to grow like an unstressed leaf. The index which used only a single, young leaf detected environmental changes with much more sensitivity. This method appeared especially useful in determining growth rates as calculated by changes in PI over time.
8 680 Vendeland et al. The Plastochron Index in Soya Bean LITERATURE CITED ACEVEDO, E., HSIAO, T. C. and HENDERSON, D. W., Immediate and subsequent growth responses of maize leaves to changes in water status. PI. Physiol. 48, BOYER, J. S., Relationship of water potential to growth of leaves. Ibid. 43, CLOUGH, B. F. and MILTHORPE, F. L., Effects of water deficit on leaf development in tobacco. Aust. J. PI. Physiol. 2, ERICKSON, R. O. and MICHEHNI, F. J., The plastochron index. Am. J. Bot. 44, FEHR,W. R., CAVINESS, C. E., BURMOOD, D. T. and PENNINGTON, J. S., 1971.Stage of development descriptions for soybean [Glycine max (L.) Merrill]. Crop Sci. 11, GATES, C. T., Water deficits and growth of herbaceous plants. In Water Deficits and Plant Growth, ed. T. T. Kozlowski. vol. 2, pp Academic Press, New York. HANADA, K. and YONG SON, S., On the expression of plant age of soybean by means of plastochron index. Proc. Crop Sci. Soc. Jap. 43, 8-28 (in Japanese). HESKETH, J. S., MYHRE, D. L. and WILEY, C. R., Temperature control of time intervals between vegetative and reproductive events in soybeans. Crop Sci. 13, HORIE, T., DEWIT, C. T., GOUDRIAAN, J. and BENSINK, J., A formal template for the development of cucumber in its vegetative stage. I. Proc. K. ned. Akad. Wet., Series C 82, HUSAIN, I. and ASPINALL, D., Water stress and apical morphogenesis in barley. Ann. Bot. 34, LAMOREAUX, R. J., CHANEY, W. R. and BROWN, K. M., The plastochron index: A review after two decades of use. Am. J. Bot. 65, MARC, J. and PALMER, J. H., Relationship between water potential and leaf and inflorescence initiation in Helianthus. Physiologia PI. 36, SILK, W. K., Plastochron indices in cantaloupe grown on an irrigation line source. Bot. Gaz. 141, THOMAS, J. F. and RAPER, C. D. Jr., Photoperiodic control of seed filling for soybeans. Crop Sci. 16, VENDELAND, J. S., Afieldevaluation of the plastochron index as a measure of the growth rate of soybeans. MS. Thesis, Cornell University, Ithaca, New York. 145 pp. WATSON, D. J. and BAPTISTE, E. C. D., A comparative physiological study of sugar-beet and mangold with respect to growth and sugar accumulation. I. Growth analysis of crop in thefield.ann. Bot. 2, WENKERT, W., LEMON, E. R. and SINCLAIR, T. R., Leaf elongation and turgor pressure in field-grown soybean. Agron. J. 70,
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