- Email: [email protected]
Reproductive development and yield components in indeterminate soybean as affected by post-flowering photoperiod
Field Crops Research 93 (2005) 212–222 www.elsevier.com/locate/fcr
Reproductive development and yield components in indeterminate soybean as affected by post-flowering photoperiod Adriana G. Kantolica,*, Gustavo A. Slaferb a
Departamento de Produccio´n Vegetal, Facultad de Agronomı´a, Universidad de Buenos Aires, Av. San Martı´n 4453, C1417DSE Buenos Aires, Argentina b Department of Crop Production and Forestry, University of Lleida, Centre UdL-IRTA, Av. Rovira Roure 191, 25198 Lleida, Spain Received 10 March 2004; received in revised form 5 October 2004; accepted 7 October 2004
Abstract Pod and seed number are the most important yield components in soybean (Glycine max (L.) Merrill) crops. Crop growth rate during post-flowering and the duration of the period when pod and seeds are formed explain much of the variation of soybean yields across genotypes and environments. Exposing post-flowering stages to long photoperiod has been found to extend the period R3–R6 and to increase seed number in soybeans grown under field conditions. In this paper, post-flowering development and yield components responses to photoperiod were quantitatively analysed and the degree of coupling between both responses was investigated. Indeterminate soybean cultivars, A-5409 (maturity group V) and Dekalb CX-458 (maturity group IV), were grown under field conditions and exposed to natural photoperiod from sowing to the beginning pod stage (R3). From then onwards, they were either kept under natural daylength or exposed to four photoperiod regimes that were artificially extended in relation to natural daylength by 1.5, 3.0, 4.5 or 6.0 h. All the extended photoperiod regimes increased the duration of R3–R6 period. Both cultivars showed a quantitative type of response through the whole range of explored photoperiods, though A-5409 exhibited a stronger sensitivity. Development responses during the R6–R8 phase were less noticeable and more variable. Exposing plants to extended photoperiod increased the number of nodes per plant and improved node fertility, thus increasing the number of pods and seeds produced per unit area. Average seed weight tended to be reduced in plants exposed to extended photoperiod and the magnitude of these effects depended both on cultivars and treatments. However, seed size was reduced in ca. 20% while seed number was increased by more than 75% due to the treatments. These results strengthen the hypothesis that manipulating photoperiod sensitivity during post-flowering in indeterminate soybean may actually be an avenue to increase seed number and yield. # 2004 Elsevier B.V. All rights reserved. Keywords: Soybean; Glycine max; Photoperiod; Development; Yield components
1. Introduction * Corresponding author. Tel.: +54 11 4524 8075; fax: +54 11 4514 8737. E-mail address: [email protected] (A.G. Kantolic).
Pod and seed number are the most important components responsible for differences in soybean
0378-4290/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.fcr.2004.10.001
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
yields between different genotypes and environments (Herbert and Litchfield, 1982; Board et al., 1999). These components are mainly determined during a period that begins sometime around flowering and extends through pod set, including the beginning of the seed-filling period (Jiang and Egli, 1995; Board and Tan, 1995; Egli, 1997). During this period, often called ‘critical period’ due to its importance for yield determination (Egli, 1998), limitations in assimilate supply reduce flower production and increase flower abortion and pod abscission (Jiang and Egli, 1993; Liu et al., 2004). A direct relationship has been found between seed number per unit area and crop growth rate during the critical period, independently of changes in growth during the rest of the cycle (Egli and Zhen-wen, 1991; Jiang and Egli, 1995; Board and Tan, 1995). More recently, a direct relationship between the duration of the critical period and seed number produced per unit area was found (Egli and Bruening, 2000; Kantolic and Slafer, 2001; Calvin˜ o et al., 2003). These findings suggest that soybean yields can be improved by placing the critical period under such conditions that both crop growth rate and duration can be increased. The duration of the reproductive period may be modified manipulating plant responses to the environmental factors controlling development, mainly temperature and photoperiod. Temperature does not only control plant development but also regulates crop growth rate (Farquhar and Sharkey, 1994). Photoperiod, instead, seems to have no major direct effects on crop growth rate but regulates the duration of most phases of soybean development (Raper and Kramer, 1987) including post-flowering phases (Thomas and Raper, 1976; Guiamet and Nakayama, 1984a; Kantolic and Slafer, 2001). There is genetic variability in plant sensitivity to photoperiod during post-flowering stages (Guiamet and Nakayama, 1984b; Summerfield et al., 1998), but it is not clear weather the sensitivity to photoperiod during the period for seed number determination is directly related with crop ability to set pods or grains. In a field study, conducted with four indeterminate genotypes, exposing the plants after R3 (beginning pod stage, in the scale of Fehr and Caviness, 1977) to photoperiods 2 h longer than the natural daylength resulted in a longer period of pod and seed formation and increased seed number (Kantolic and Slafer, 2001).
213
These increments were evident in early sowing dates but were not very noticeable when the sowing was delayed, suggesting that the range of natural photoperiods explored by the plants during the reproductive phases conditioned the responses to treatments. There are some reports in the literature showing that soybean development responds quantitatively to photoperiod after flowering (Grimm et al., 1994; Summerfield et al., 1998). However, we are aware of no evidence of any quantitative response of seed number to a steadily increased duration of the critical period due to photoperiodic effects. As the reproductive period of soybean can be exposed to environments with daylengths varying from 12 to more than 16 h, depending on the latitude and time of growth, it becomes relevant to explore the limits of photoperiodic improvement of seed number under field conditions. The aim of this paper was to quantify both development and seed production responses to photoperiod during post-flowering, independently of any responses during vegetative phases, in order to shed some light on the degree of coupling between both responses in field grown soybeans.
2. Materials and methods 2.1. Culture Two commercial indeterminate soybean cultivars, A-5409 (maturity group V) and Dekalb-CX-458 (maturity group IV), were grown under field conditions at the Experimental Site of the Faculty of Agronomy, University of Buenos Aires (348350 S, 588290 W), during the 1999/2000 growing season. The cultivars were selected considering previous results, as they exhibited a relatively strong sensitivity to photoperiod in the reproductive development within their maturity group, beyond responses to this factor in vegetative phases (Kantolic and Slafer, 2001). The soil was a silty clay loam classified as Vertic Argiudol. Seeds were inoculated with Bradyrhizobium liquid inoculant and hand sown at a high-planting rate in field plots. When the unifoliate leaves were expanded, the plots were hand-thinned to obtain a uniform plant population of 45 plants per m2, a population capable of attaining 95% of radiation interception at flowering. In order to make both cultivars flower in the closest
214
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
possible date, and based on experience from previous studies, they were sown on 26 November (A-5409) and on 16 December (Dekalb-CX-458). To minimize stresses as much as possible, fungal diseases were prevented by spraying recommended fungicides, while weeds and insect pests were controlled with conventional herbicides and insecticides. Plots were irrigated whenever natural rainfall had to be supplemented to prevent water limitations. 2.2. Treatments and experimental design Treatments consisted of the factorial combination of the two above-mentioned cultivars and five photoperiod regimes established from R3 onwards. The treatments were arranged in a split-plot design, with three replicates; photoperiod treatments were assigned to main plots and the cultivars were randomized in subplots consisting of five rows, 0.35 m apart and 2.5 m long. To attain the photoperiod treatments, plants were grown under natural photoperiod from sowing to beginning pod stage (R3, as described by Fehr and Caviness, 1977). From then onwards, they were either kept under natural daylength (DNAT) or exposed to four photoperiod regimes that were artificially extended, in relation to natural daylength by 1.5, 3.0, 4.5 or 6.0 h (D+1.5, D+3.0, D+4.5, D+6.0, respectively) mimicking the natural daylength change. The moment of application of the treatment and the range of explored photoperiods were chosen in order to avoid a delay of first flowering and to prevent the flowering reversion phenomenon (Washburn and Thomas, 2000). To extend the daylength in the field plots, portablelighting structures like those described earlier (Kantolic and Slafer, 2001) were used. Each structure combined incandescent and fluorescent lamps that provided a mean photosynthetic photon flux density of 2.7 mmol m2 s1 and a red: far red quantum ratio (R:FR) of 1.11. Light intensity and quality were measured at the canopy surface at night with a LICOR line quantum sensor (LI-COR Inc., Lincoln, NE) and a 660/730 Sensor SKR 110 (Skye Instrument Ltd., Powys, UK), respectively. During the treatment imposition, lights were automatically turned on before sunset and off at the required time depending on the length of extension. To calculate photoperiod both civil twilights (the period beginning or ending when
the center of the sun is geometrically 68 below the horizon) were taken into account. 2.3. Data collection and analysis Phenological stages (Fehr and Caviness, 1977) were recorded at 1–3-day intervals in a previously defined area of three bordered rows of 0.50 m long in each subplot. The timing of a particular developmental stage was determined as the date when 50% of the plants of the monitored area reached it. Durations of R1–R3, R3–R6 and R6–R8 were computed for each subplot. At maturity, two adjacent rows of 1 m long were harvested and the number of nodes, pods and seeds were counted. The number of seeds per node was calculated at a whole plant level, relating seed number and total node number per plant. Average seed weight was estimated from three randomly taken sub-samples of 100 seeds per subplot. 2.4. Meteorological data and calculations Data of daily global solar radiation and maximum and minimum temperatures were obtained from a standard meteorological station located ca. 300 m away from the plots, estimating daily mean temperature as the average between maximum and minimum. The integral of solar radiation during the period for seed formation was calculated as the sum of daily incident global radiation between R3 and R6 stages. To separate thermal and photoperiodic effects on development, the duration of R3–R6 period was corrected using a linear three-segmented function (Piper et al., 1996) considering that the rate of development on day t [D(t)] is a function of temperature: DðtÞ ¼ 0 ðT TbÞ DðtÞ ¼ ðTo1 TbÞ DðtÞ ¼ 1 ðTm TÞ DðtÞ ¼ ðTm To2Þ DðtÞ ¼ 0
if T < Tb if Tb < T < To1 if To1 < T < To2
(1)
if To2 < T < Tm if T > Tm
where T is daily mean temperature, Tb = base temperature below which there is no development, To1 = lower optimum temperature, To2 = upper optimum temperature, and Tm = maximum temperature,
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
above which there is no development. According to Piper et al. (1996), cardinal temperatures for the subperiod R3–R5 were Tb = 2.5 8C, To1 = 25 8C, To2 = 30 8C and Tm = 55 8C. From R5 onwards, Tb was 48 8C and To1 was 28 8C. According to Eq. (1), one thermal day is equal to one calendar day when temperature is optimum and varies between zero and one outside this range. The accumulated thermal days between two stages, e.g. R3 and R6, represented the corrected duration of the phase, R3–R6. Considering that low temperatures may promote flower abortion and pod abscission, we defined an effective time for pod addition as the period thermally adequate for setting pods. It was estimated computing the accumulated thermal days between R3 and R6, using Eq. (1) with the cardinal temperatures proposed by Boote et al. (1997) for the pod addition process: Tb = 14 8C, To1 = 21.5 8C, To2 = 26.5 8C and Tm = 40 8C. To evaluate the possible joint effects of radiation and temperature on seed number, we defined the effective radiation on day t [ER(t)] as: ERðtÞ ¼ DðtÞRðtÞ
(2)
215
where D(t) is the rate of development on day t, estimated with Eq. (1) using the cardinal temperatures proposed for the pod addition process, and R(t) is the daily incident global radiation. The sum of ER(t) from R3 to R6, was defined as the effective radiation accumulated in the critical period. Each calculation was independently performed for each subplot. Results were compared with those previously obtained with the same genotypes in an independent experiment carried out a year before, in which photoperiod was extended only by 2 h in relation to natural daylength (Kantolic and Slafer, 2001).
3. Results 3.1. Development All the extended photoperiod regimes increased the duration of the R3–R6 period for both genotypes (Table 1). Both cultivars showed a quantitative type of response throughout the whole range of explored photoperiods, though the cultivar A-5409, exhibited a stronger response than that of Dekalb-CX-458.
Table 1 Duration and average temperatures of R3–R6 and R6–R8 periods of soybean grown under natural photoperiod (DNAT) or exposed to artificially extended photoperiods 1.5, 3.0, 4.5 or 6.0 h longer than natural (D+1.5 through D+6.0) between R3 stage and physiological maturity R3–R6 Duration (days) A-5409 DNAT D+1.5 D+3.0 D+4.5 D+6.0 Dekalb-CX-458 DNAT D+1.5 D+3.0 D+4.5 D+6.0 LSDa LSDb MSc photoperiod MSc cultivar MSc interaction a b c
R6–R8 Temperature (8C)
Duration (days)
Temperature (8C)
34.0 52.7 76.7 91.0 100.3
24.2 22.5 21.7 20.9 20.2
19.0 30.0 29.3 28.7 21.7
22.0 16.9 15.3 15.0 12.3
31.0 37.7 45.0 53.3 64.3
24.3 24.3 23.9 23.0 22.1
15.0 43.3 52.0 58.0 51.0
23.3 19.9 17.6 16.6 15.8
2.6 2.4 2477** 4838** 266**
0.6 0.6 17.2** 15.0** 1.4**
9.3 11.1 645** 2484** 297**
1.3 1.2 56.5** 22.4* 0.6 ns
LSD (p = 0.05) between means, within photoperiod treatments. LSD (p = 0.05) between means, between photoperiod treatments. Mean square of the analysis of variance and significance of the principal effects and interactions (**p < 0.01; *p < 0.05; ns: not significant).
216
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
As plants were grown under field conditions, the delay in reaching the R6 stage resulted in a decrease of average temperature for the R3–R6 period (Table 1). For that reason, the right estimation of photoperiod sensitivity required taking into account thermal effects on developmental rate. When relating corrected duration of R3–R6 with average photoperiod, a typical short-day response was evident for both cultivars (Fig. 1), that closely matched previous results (open symbols in Fig. 1). Although greater sensitivity of A-5409 remained evident, its sensitivity was not constant across the whole range of explored photoperiods (Fig. 1). Development responses during the R6–R8 phase resulted less noticeable and more variable. Longer durations were obtained in Dekalb-CX-458 under long photoperiods (Table 1) but the response of both cultivars was not quantitative across the whole range of explored photoperiods (Fig. 2).
photoperiod. In average, plants grown under extended photoperiod produced ca. 75% more seeds than plants grown under natural photoperiod. In Dekalb-CX-458, maximum number of seeds was produced in plants grown under the three most extended photoperiod regimes, without significant differences between them. For this cultivar, plants grown under the most extended photoperiod produced twice the number of seeds as the control plants. Exposure to extended photoperiods increased the number of nodes both in the mainstem and in the branches, with a stronger response in A-5409 (Fig. 3). In both cultivars, a slight but significant increase in the number of seeds per node was produced under extended photoperiods (Table 2).
3.2. Number of seeds
The relationship between seed number and the duration of R3–R6 was curvilinear (Fig. 4) as a result of the quantitative response in the duration of R3–R6 stage combined with the absence of differences in the number of seeds and pods produced between the most extended photoperiod regimes. To explore whether this apparent saturation in the response of seed number to the length of the R3–R6 period for the longest durations could be related, at
Exposing plants to extended photoperiod after R3 increased the number of pods and seeds, without consistent changes in seed number per pod (Table 2). In A-5409, there were no differences in pod and seed number between the four regimes of extended
Fig. 1. Relationship between the duration of the period R3–R6 corrected by temperature and mean photoperiod for A-5409 (diamonds) and Dekalb CX 458 (triangles). Open symbols correspond to previous results (Kantolic and Slafer, 2001). Vertical bars represent the standard error of the means and are shown when bigger than symbols. Duration of the R3–R6 period was corrected using cardinal temperatures proposed by Piper et al. (1996).
3.3. Relationship between the duration of the critical period and the number of seeds
Fig. 2. Relationship between the corrected duration of the period R6–R8 and mean photoperiod for A-5409 and Dekalb CX 458. Symbols as in Fig. 1. Duration of the R6–R8 period was corrected using cardinal temperatures proposed by Piper et al. (1996).
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
217
Table 2 Average number of pods and seeds per square meter and number of seeds per pod and per node, in soybean plants grown under natural photoperiod (DNAT) or exposed to artificially extended photoperiods 1.5, 3.0, 4.5 o 6.0 h longer than natural (D+1.5 through D+6.0) between R3 stage and physiological maturity Number of pods (m2)
Number of seeds (m2)
(pod1)
(node1)
A-5409 DNAT D+1.5 D+3.0 D+4.5 D+6.0
1659 2649 3189 2801 2724
3705 6346 6677 6526 6300
2.2 2.4 2.3 2.3 2.3
3.1 3.6 3.7 3.2 3.4
Dekalb CX-458 DNAT D+1.5 D+3.0 D+4.5 D+6.0
773 1323 1834 1883 1841
2102 3439 4330 4748 4895
2.6 2.4 2.4 2.5 2.7
2.3 3.1 3.2 3.5 3.8
646 658 1575418** 8644755** 126303 ns
1619 1143 8066973** 30236464** 563986 ns
0.1 0.2 0.01 ns 0.47** 0.03*
0.5 0.6 0.758** 0.367 ns 0.423 ns
LSD 1a LSD 2b MSc photoperiod MS cultivar MS interaction a b c
Least significant difference (p = 0.05) between means, within photoperiod treatments. Least significant difference (p = 0.05) between means, between photoperiod treatments. Mean square of the analysis of variance and significance of the principal effects and interactions (**p < 0.01; *p < 0.05; ns: not significant).
least partly, to environmental limitations, we analyzed how long increments in R3–R6 duration really implied more time to grow and set pods. Due to the fact that temperatures and radiation steadily decreased as the
season progressed, the longest durations of R3–R6 did not represent important increments in radiation capture nor did they extend the effective time for pod addition (Fig. 5).
Fig. 3. Number of nodes in mainstem (solid bars) and in branches (open bars) in soybean plants grown under natural or artificially extended photoperiods. Under each bar, the hours of extension of photoperiod applied is shown. Vertical lines show the standard error of the means.
Fig. 4. Relationship between the number of seeds per square meter and the duration of the R3–R6 period for A-5409 and Dekalb CX 458. Symbols as in Fig. 1.
218
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
seed weight, when occurred, were far smaller than increases in number of seeds per unit land area.
4. Discussion
Fig. 5. Relationship between the increments in the effective time for pod addition (closed symbols) and in accumulated radiation (open symbols) during R3–R6 and the increments in duration of this phase produced by photoperiod extensions, for A-5409 (diamonds) and Dekalb CX458 (triangles). Increments are expressed in relative terms to the environmental conditions explored in the plants exposed to natural photoperiod. The effective time for pod addition was estimated according to the cardinal temperature proposed by Boote et al. (1997) for the pod addition process, as explained in the text. The dotted line represents the 1:1 relationship.
3.4. Seed weight Average seed weight tended to be reduced in plants exposed to extended photoperiod and the magnitude of these effects depended both on cultivars and photoperiod regimes. Extending photoperiod in 1.5 h slightly reduced seed weight only in A-5409 while the longest extension reduced seed weight by ca. 20% in both cultivars (Fig. 6). In any case, reductions in
Fig. 6. Average seed weight of soybean plants exposed to different photoperiods from R3 to maturity. Vertical lines show the standard error of the means.
Photoperiod modified the duration of the critical period for seed determination in both indeterminate soybean cultivars and this response was evident over a wide range of photoperiods. Photoperiodic effects during post-flowering phases have been previously reported (Thomas and Raper, 1976; Guiamet and Nakayama, 1984a,b; Morandi et al., 1990; Summerfield et al., 1998; Ellis et al., 2000; Kantolic and Slafer, 2001). The results of the present study showed that this response is quantitative even at photoperiods longer than those generally explored by soybean crops grown commercially. Cultivar A-5409 expressed a greater sensitivity to photoperiod during reproductive period than Dekalb-CX-458, confirming initial results from which these cultivars were selected for this study (Kantolic and Slafer, 2001). Plants exposed to longer photoperiods produced more nodes although the extension of daylength began, in average, as late as 18 days after first flowering. The terminal apex of indeterminate soybeans may become reproductive even after R1 stage (Caffaro et al., 1988) so that the increased node number in response to extended photoperiod may reflect that the apex was still able to respond to changes in daylength even after the R3 stage. Moreover, long photoperiods have been found to promote the elongation of internodes and dry matter partitioning towards vegetative organs, thus allowing more growth of the differentiated internodes (Caffaro et al., 1988). Photoperiodic effects on branch growth have been previously reported (Board and Settimi, 1986; Caffaro and Nakayama, 1988; Kantolic and Slafer, 2001), although it remains unclear whether the increased number of branch nodes was a result of a development effect (i.e. more days were available for internodes to be differentiated and elongated) or a consequence of more growth due to a longer period intercepting radiation (more carbohydrates were available for vegetative organs to grow). In the present study, the increment in node number was evident only between plants from natural and extended photoperiods, while there was no difference between the four extended photoperiod regimes. These findings contrast with the
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
quantitative response in the developmental rate. Although our study was not designed to investigate photoperiodic control of node number, the absence of a quantitative response suggests that other factors, besides those controlling node differentiation, may be involved in determining the final number of nodes. Minor changes occurred in seed number per pod in response to photoperiod extension, in coincidence with previous results (Kantolic and Slafer, 2001). Similar findings of small or no significant changes in seed number per pod have been reported in studies that manipulated incident radiation (Schou et al., 1978; Mathew et al., 2000), plant population (Dominguez and Hume, 1978) or canopy architecture (Board et al., 1996), confirming the remarkably high stability of this yield component and its minor importance in defining seed number per unit land area and yield across environments. Increased node fertility, expressed as seed number per node in response to extended photoperiod, was therefore a consequence of an increase in pod number per node. This has been also found in our previous study (Kantolic and Slafer, 2001) and several papers highlighted the relevance of this yield component in determining soybean yield (e.g. Board et al., 1999; Ball et al., 2001). Pod number per node is the result of the balance between the generation and the mortality of flowers and pods. The generation of pods includes the initiation of flower buds and their development into mature flowers. Both processes are affected by photoperiod (Thomas and Kanchanapoom, 1991; Zhang et al., 2001). However, the production of more flowers does not warrant an increase in the number of pods, as enlarging pods can fail to set (Westgate and Peterson, 1993). Both the production and the abortion of mature flowers and young pods are sensitive to changes in photosynthate supply during flowering and pod set (Jiang and Egli, 1993; Bruening and Egli, 1999, 2000). This means that if exposure to extended photoperiod could enhance seed number per node, its effects should somehow improve the balance between source strength and sink demand, preventing abortion. The relationship between seed number and the duration of R3–R6 was curvilinear, suggesting some kind of saturation of the response at durations longer than a threshold. However, because of the delay in development itself produced by the longest daylengths, further lengthening the R3–R6 phase beyond that
219
threshold did not represent actual increases in the radiation available for growth nor in the time thermally effective to set pods. Pod addition is highly sensitive to low temperatures (Thomas and Raper, 1976; Hume and Jackson, 1981) while low radiation reduces pod number through reductions of crop growth rate (Board et al., 1992). This means that the improving of seed number by increasing the duration of R3–R6 through photoperiod, should be conditioned to a concomitant improvement in crop growth and partitioning to pods. Rearranging our results and relating seed number with the radiation accumulated during R3–R6 (Fig. 7a) or with the duration of R3–R6 corrected by temperature (Fig. 7b), reduced the curvilinearity evidenced in A-5409 when seed number was related to duration of R3–R6 (Fig. 4). When both thermal and radiation conditions were jointly taken into account by estimating the effective radiation for the R3–R6 period, the differences between treatments of extended photoperiod disappeared and the relationship became mostly linear (Fig. 7c). This linearity, compared with the curvilinear relationship when using duration as the independent variable, suggests that even though more days elapsed to complete the R3–R6 phase under the longest photoperiods, this latter lengthening of the critical phase did not imply differences in conditions for pod growth. In the present study, average seed weight was reduced in the treatments of extended photoperiod, mainly in A-5409. Exposure to long photoperiods has been found to reduce seed growth rate and final seed weight in controlled environments (Raper and Thomas, 1978; Morandi et al., 1988). However, other causes beyond direct photoperiod effects may be involved in this study. As the length of R3–R6 increased by photoperiodic effects, the seed growth period was delayed into worse environmental conditions (lower temperature and lower radiation). Low temperatures reduce seed growth rate (Egli, 1998) and the average temperature was lower during the seedfilling period of plants exposed to longer photoperiods from R3 onwards. It is known that seed growth is usually limited by assimilate supply (Egli, 1999), though it seems to be a large variability in the degree of source limitation for seed filling in soybean (Borra´ s et al., 2004). In the preset study, comparing the extreme treatments, seed size was reduced by ca. 20% while seed number was increased by more than 75%. Thus, if a competitive relationship was established
220
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
Fig. 7. Relationship between: the number of seeds and (i) accumulated solar radiation between R3 and R6 stages (a); (ii) the duration of R3–R6 corrected by thermal conditions for pod addition equations (b); and (iii) radiation powered by thermal conditions (effective radiation, panel c). Symbols as in Fig. 1. Temperature coefficients for correcting the duration of R3–R6 and powering radiation were taken from Boote et al. (1997).
between the growing seeds during the seed-filling phase, it was not mutually exclusive, and yield was undoubtedly improved by exposing plants to longer photoperiod after R3. It must be noted, however, that probable applications of our finding include genetic manipulation of crop sensitivity to photoperiod, developing cultivars that flower earlier and extend the post-flowering period (Kantolic and Slafer, 2001), thus seed filling should not occur under unfavorable
conditions. In this context, emphasis should be put on improving the understanding of photoperiodic effects on pod and seed number. The fact that seed number increased under long photoperiods only when more radiation was available and that the relationship between the number of seeds and their average size was not completely competitive, reinforce the hypothesis that photoperiod effects on seed number should include mechanisms related with carbon metabolism. Although the nature of the mechanisms remains unclear, they should include any or both of the regulation components of pod and seed set (Egli and Bruening, 2002a): the supply of assimilates from photosynthesis and the utilization of assimilates by the seeds. In this study, it can be assumed that the daily supply of assimilates has been maximized, as maximum interception of radiation was achieved at the beginning of the reproductive period and stresses were avoided. However, we cannot discard possible effects of the treatments on the distribution of assimilates within the plants. One critical aspect of assimilate utilization seems to be the simultaneous growth of pods of widely different ages, as the rapid growth of older pods may reduce assimilate supply to flowers and young pods, triggering their abortion (Egli and Bruening, 2002b). Although photoperiod is known to modify the dynamics of flower production and pod growth under controlled environment (Guiamet and Nakayama, 1984a; Morandi et al., 1990), it is not clear if this mechanism may be underlying the responses observed in the current investigation. Evidently, more research in intact plants grown in the field is needed to clarify whether photoperiod increases seed number through increasing assimilate availability (as a longer R3–R6 period may result in greater total radiation interception and greater production of assimilates) or also by reducing instantaneous sink demand, by modifying timing of flowers and pod production. Experiments consisting of the factorial combination of photoperiod extensions and shading in field plots may help solve this issue.
Acknowledgements We gratefully acknowledge the support given by competitive grants from both Agencia Nacional de
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
Promocion Cientifica y Tecnologica (FONCyT program) and Universidad de Buenos Aires (UBACyT program). GAS was working at the Universidad de Buenos Aires and CONICET during the experimental growing seasons and at ICREA/Universitat de Lleida during final analysis of results and writing of the ms.
References Ball, R.A., McNew, R.W., Vories, E.D., Keisling, T.C., Purcell, L.C., 2001. Path analyses of population density effects on short-season soybean yield. Agron. J. 3, 187–195. Board, J.E., Settimi, J.R., 1986. Photoperiod effect before and after flowering on branch development in determinate soybean. Agron. J. 78, 995–1002. Board, J.E., Tan, Q., 1995. Assimilatory capacity effects on soybean yield components and pod number. Crop Sci. 35, 846–851. Board, J.E., Kamal, M., Harville, B.G., 1992. Temporal importance of greater light interception to increased yield in narrow-row soybean. Agron. J. 84, 575–579. Board, J.E., Zhang, W., Harville, B.G., 1996. Yield rankings for soybean cultivars grown in narrow and wide rows with late planting dates. Agron. J. 88, 240–245. Board, J.E., Kang, M.S., Harville, B.G., 1999. Path analyses of the yield formation process for late-planted soybean. Agron. J. 91, 128–135. Boote, K.J., Jones, J.W., Hoogenboom, G., 1997. Simulation of crop growth: CROPGRO model. In: Peart, R.M., Curry, R.B. (Eds.), Agricultural Systems Modeling. Marcel Dekker, NY, pp. 651– 692. Borra´ s, L., Slafer, G.A., Otegui, M., 2004. Seed dry weight response to source-sink manipulations in wheat, maize and soybean: a quantitative reappraisal. Field Crops Res. 86, 131–146. Bruening, W.P., Egli, D.B., 1999. Relationship between photosynthesis and seed number at phloem isolated nodes in soybean. Crop Sci. 39, 1769–1775. Bruening, W.P., Egli, D.B., 2000. Leaf starch accumulation and seed set at phloem- isolated nodes in soybean. Field Crops Res. 68, 113–120. Caffaro, S.V., Nakayama, F., 1988. Vegetative activity of the main stem terminal bud under photoperiod and flower removal treatments in soybean. Aust. J. Plant Physiol. 15, 475–480. Caffaro, S.V., Martignone, R.A., Torres, R., Nakayama, F., 1988. Photoperiod regulation of vegetative growth and meristem behavior toward flower initiation of an indeterminate soybean. Bot. Gaz. 149, 311–316. Calvin˜ o, P.A., Sadras, V.O., Andrade, F.H., 2003. Development, growth and yield of late-sown soybeans in the southern Pampas. Eur. J. Agron. 19, 265–275. Dominguez, C., Hume, D.J., 1978. Flowering, abortion and yield of early maturing soybeans at three densities. Agron. J. 70, 801– 805. Egli, D.B., 1997. Cultivar maturity and response of soybean to shade stress during seed filling. Field Crops Res. 52, 1–8.
221
Egli, D.B., 1998. Seed Biology and the Yield of Grain Crops. CAB International, UK. Egli, D.B., 1999. Variation in leaf starch and sink limitations during seed filling in soybean. Crop Sci. 39, 1361–1368. Egli, D.B., Zhen-wen, Y., 1991. Crop growth rate and seeds per unit area in soybeans. Crop Sci. 31, 439–442. Egli, D.B., Bruening, W.P., 2000. Potential of early-maturing soybean cultivars in late plantings. Agron. J. 92, 532–537. Egli, D.B., Bruening, W.P., 2002a. Synchronous flowering and fruit set at phloem-isolated nodes in soybean. Crop Sci. 42, 1535– 1540. Egli, D.B., Bruening, W.P., 2002b. Flowering and fruit set dynamics at phloem-isolated nodes in soybean. Field Crops Res. 79, 9–19. Ellis, R.H., Asumadu, H., Qi, A., Summerfield, R.J., 2000. Effects of photoperiod and maturity genes on plant growth, partitioning, radiation use efficiency and yield in soyabean [Glycine max (L.) Merrill] ‘Clark’. Ann. Botany 85, 335–343. Farquhar, G.D., Sharkey, T.D., 1994. Photosynthesis and carbon assimilation. In: Boote, K.J., Bennet, J.M., Sinclair, T.R., Paulsen, G.M. (Eds.), Physiology and Determination of Crop Yield. ASA CSSA SSSA, Madison, WI, pp. 187–210. Fehr, W.R., Caviness, C.E., 1977. Stages of soybean development. Spec. Rep. 80, Iowa State University, Ames, Iowa. Grimm, S.S., Jones, J.W., Boote, K.J., Herzog, D.C., 1994. Modeling the occurrence of reproductive stages after flowering for four soybean cultivars. Agron. J. 86, 31–38. Guiamet, J.J., Nakayama, F., 1984a. The effects of long days upon reproductive growth in soybeans (Glycine max (L.) Merr.) cv. Williams. Jpn. J. Crop Sci. 53, 35–40. Guiamet, J.J., Nakayama, F., 1984b. Varietal responses of soybeans (Glycine max (L.) Merr.) to long days during reproductive growth. Jpn. J. Crop Sci. 53, 299–306. Herbert, S.J., Litchfield, G.V., 1982. Partitioning soybean seed yield components. Crop Sci. 22, 1074–1079. Hume, D.J., Jackson, A.K.H., 1981. Pod formation in soybeans at low temperature. Crop Sci. 21, 933–937. Jiang, H., Egli, D.B., 1993. Shade induced changes in flower and pod number and flower and fruit abscission in soybean. Agron. J. 85, 221–225. Jiang, H., Egli, D.B., 1995. Soybean seed number and crop growth rate during flowering. Agron. J. 87, 264–267. Kantolic, A.G., Slafer, G.A., 2001. Photoperiod sensitivity after flowering and seed number determination in indeterminate soybean cultivars. Field Crops Res. 72, 109–118. Liu, F., Jensen, C.R., Anderson, M.N., 2004. Drought stress effect on carbohydrate concentration in soybean leaves and pods during early reproductive development: its implication in altering pod set. Field Crops Res. 86, 1–13. Mathew, J.P., Herbert, S.J., Zhang, S., Rautenkranz, A.A.F., Litchfield, G.V., 2000. Differential response of soybean yield components to the timing of light enrichment. Agron. J. 92, 1156– 1161. Morandi, E.N., Casano, L.M., Reggiardo, L.M., 1988. Post-flowering photoperiodic effect on reproductive efficiency and seed growth in soybean. Field Crops Res. 18, 227–241. Morandi, E.N., Schussler, J.R., Brenner, M.L., 1990. Photoperiodically induced changes in seed growth rate of soybean as related
222
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
to endogenous concentrations of ABA and sucrose in seed tissues. Ann. Bot. 66, 605–611. Piper, E., Boote, K.J., Jones, J.W., Grimm, S.S., 1996. Comparison of two phenology models for predicting flowering and maturity date of soybean. Crop Sci. 36, 1606–1614. Raper, C.D., Thomas, J.F., 1978. Photoperiodic alteration of dry matter partitioning and seed yield in soybeans. Crop Sci. 18, 654–656. Raper, C.D., Kramer, P.J., 1987. Stress physiology. In: Wilcox, J.R. (Ed.), Soybeans: Improvement, Production and Uses. second ed. ASA CSSA SSA, Madison, WI, agronomy monograph no. 16, pp. 589–641. Schou, J.B., Jeffers, D.L., Streeter, J.G., 1978. Effects of reflectors, black boards, or shades applied at different stages of plant development on yield of soybeans. Crop Sci. 18, 29–34. Summerfield, R.J., Asumadu, H., Ellis, R.H., Qi, A., 1998. Characterization of the photoperiodic response of post-flowering
development in maturity isolines of soyabean [Glycine max (L.) Merrill] ‘Clark’. Ann. Botany 82, 765–771. Thomas, J.F., Raper Jr., C.D., 1976. Photoperiodic control of seed filling for soybeans. Crop Sci. 16, 667–672. Thomas, J.F., Kanchanapoom, M.L., 1991. Shoot meristem activity during floral transition in Glycine max (L.) Merr. Bot. Gaz. 152, 139–147. Washburn, C.F., Thomas, J.F., 2000. Reversion of flowering in Glycine max (Fabaceae). Am. J. Bot. 87, 1425–1438. Westgate, M.E., Peterson, C.M., 1993. Flower and pod development in water-deficient soybeans (Glycine max L. Merr). J. Exp. Bot. 44, 109–117. Zhang, L., Wang, R., Hesketh, J.D., 2001. Effects of photoperiod on growth and development of soybean floral bud in different maturity. Agron. J. 63, 944–948.
Reproductive development and yield components in indeterminate soybean as affected by post-flowering photoperiod Adriana G. Kantolica,*, Gustavo A. Slaferb a
Departamento de Produccio´n Vegetal, Facultad de Agronomı´a, Universidad de Buenos Aires, Av. San Martı´n 4453, C1417DSE Buenos Aires, Argentina b Department of Crop Production and Forestry, University of Lleida, Centre UdL-IRTA, Av. Rovira Roure 191, 25198 Lleida, Spain Received 10 March 2004; received in revised form 5 October 2004; accepted 7 October 2004
Abstract Pod and seed number are the most important yield components in soybean (Glycine max (L.) Merrill) crops. Crop growth rate during post-flowering and the duration of the period when pod and seeds are formed explain much of the variation of soybean yields across genotypes and environments. Exposing post-flowering stages to long photoperiod has been found to extend the period R3–R6 and to increase seed number in soybeans grown under field conditions. In this paper, post-flowering development and yield components responses to photoperiod were quantitatively analysed and the degree of coupling between both responses was investigated. Indeterminate soybean cultivars, A-5409 (maturity group V) and Dekalb CX-458 (maturity group IV), were grown under field conditions and exposed to natural photoperiod from sowing to the beginning pod stage (R3). From then onwards, they were either kept under natural daylength or exposed to four photoperiod regimes that were artificially extended in relation to natural daylength by 1.5, 3.0, 4.5 or 6.0 h. All the extended photoperiod regimes increased the duration of R3–R6 period. Both cultivars showed a quantitative type of response through the whole range of explored photoperiods, though A-5409 exhibited a stronger sensitivity. Development responses during the R6–R8 phase were less noticeable and more variable. Exposing plants to extended photoperiod increased the number of nodes per plant and improved node fertility, thus increasing the number of pods and seeds produced per unit area. Average seed weight tended to be reduced in plants exposed to extended photoperiod and the magnitude of these effects depended both on cultivars and treatments. However, seed size was reduced in ca. 20% while seed number was increased by more than 75% due to the treatments. These results strengthen the hypothesis that manipulating photoperiod sensitivity during post-flowering in indeterminate soybean may actually be an avenue to increase seed number and yield. # 2004 Elsevier B.V. All rights reserved. Keywords: Soybean; Glycine max; Photoperiod; Development; Yield components
1. Introduction * Corresponding author. Tel.: +54 11 4524 8075; fax: +54 11 4514 8737. E-mail address: [email protected] (A.G. Kantolic).
Pod and seed number are the most important components responsible for differences in soybean
0378-4290/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.fcr.2004.10.001
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
yields between different genotypes and environments (Herbert and Litchfield, 1982; Board et al., 1999). These components are mainly determined during a period that begins sometime around flowering and extends through pod set, including the beginning of the seed-filling period (Jiang and Egli, 1995; Board and Tan, 1995; Egli, 1997). During this period, often called ‘critical period’ due to its importance for yield determination (Egli, 1998), limitations in assimilate supply reduce flower production and increase flower abortion and pod abscission (Jiang and Egli, 1993; Liu et al., 2004). A direct relationship has been found between seed number per unit area and crop growth rate during the critical period, independently of changes in growth during the rest of the cycle (Egli and Zhen-wen, 1991; Jiang and Egli, 1995; Board and Tan, 1995). More recently, a direct relationship between the duration of the critical period and seed number produced per unit area was found (Egli and Bruening, 2000; Kantolic and Slafer, 2001; Calvin˜ o et al., 2003). These findings suggest that soybean yields can be improved by placing the critical period under such conditions that both crop growth rate and duration can be increased. The duration of the reproductive period may be modified manipulating plant responses to the environmental factors controlling development, mainly temperature and photoperiod. Temperature does not only control plant development but also regulates crop growth rate (Farquhar and Sharkey, 1994). Photoperiod, instead, seems to have no major direct effects on crop growth rate but regulates the duration of most phases of soybean development (Raper and Kramer, 1987) including post-flowering phases (Thomas and Raper, 1976; Guiamet and Nakayama, 1984a; Kantolic and Slafer, 2001). There is genetic variability in plant sensitivity to photoperiod during post-flowering stages (Guiamet and Nakayama, 1984b; Summerfield et al., 1998), but it is not clear weather the sensitivity to photoperiod during the period for seed number determination is directly related with crop ability to set pods or grains. In a field study, conducted with four indeterminate genotypes, exposing the plants after R3 (beginning pod stage, in the scale of Fehr and Caviness, 1977) to photoperiods 2 h longer than the natural daylength resulted in a longer period of pod and seed formation and increased seed number (Kantolic and Slafer, 2001).
213
These increments were evident in early sowing dates but were not very noticeable when the sowing was delayed, suggesting that the range of natural photoperiods explored by the plants during the reproductive phases conditioned the responses to treatments. There are some reports in the literature showing that soybean development responds quantitatively to photoperiod after flowering (Grimm et al., 1994; Summerfield et al., 1998). However, we are aware of no evidence of any quantitative response of seed number to a steadily increased duration of the critical period due to photoperiodic effects. As the reproductive period of soybean can be exposed to environments with daylengths varying from 12 to more than 16 h, depending on the latitude and time of growth, it becomes relevant to explore the limits of photoperiodic improvement of seed number under field conditions. The aim of this paper was to quantify both development and seed production responses to photoperiod during post-flowering, independently of any responses during vegetative phases, in order to shed some light on the degree of coupling between both responses in field grown soybeans.
2. Materials and methods 2.1. Culture Two commercial indeterminate soybean cultivars, A-5409 (maturity group V) and Dekalb-CX-458 (maturity group IV), were grown under field conditions at the Experimental Site of the Faculty of Agronomy, University of Buenos Aires (348350 S, 588290 W), during the 1999/2000 growing season. The cultivars were selected considering previous results, as they exhibited a relatively strong sensitivity to photoperiod in the reproductive development within their maturity group, beyond responses to this factor in vegetative phases (Kantolic and Slafer, 2001). The soil was a silty clay loam classified as Vertic Argiudol. Seeds were inoculated with Bradyrhizobium liquid inoculant and hand sown at a high-planting rate in field plots. When the unifoliate leaves were expanded, the plots were hand-thinned to obtain a uniform plant population of 45 plants per m2, a population capable of attaining 95% of radiation interception at flowering. In order to make both cultivars flower in the closest
214
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
possible date, and based on experience from previous studies, they were sown on 26 November (A-5409) and on 16 December (Dekalb-CX-458). To minimize stresses as much as possible, fungal diseases were prevented by spraying recommended fungicides, while weeds and insect pests were controlled with conventional herbicides and insecticides. Plots were irrigated whenever natural rainfall had to be supplemented to prevent water limitations. 2.2. Treatments and experimental design Treatments consisted of the factorial combination of the two above-mentioned cultivars and five photoperiod regimes established from R3 onwards. The treatments were arranged in a split-plot design, with three replicates; photoperiod treatments were assigned to main plots and the cultivars were randomized in subplots consisting of five rows, 0.35 m apart and 2.5 m long. To attain the photoperiod treatments, plants were grown under natural photoperiod from sowing to beginning pod stage (R3, as described by Fehr and Caviness, 1977). From then onwards, they were either kept under natural daylength (DNAT) or exposed to four photoperiod regimes that were artificially extended, in relation to natural daylength by 1.5, 3.0, 4.5 or 6.0 h (D+1.5, D+3.0, D+4.5, D+6.0, respectively) mimicking the natural daylength change. The moment of application of the treatment and the range of explored photoperiods were chosen in order to avoid a delay of first flowering and to prevent the flowering reversion phenomenon (Washburn and Thomas, 2000). To extend the daylength in the field plots, portablelighting structures like those described earlier (Kantolic and Slafer, 2001) were used. Each structure combined incandescent and fluorescent lamps that provided a mean photosynthetic photon flux density of 2.7 mmol m2 s1 and a red: far red quantum ratio (R:FR) of 1.11. Light intensity and quality were measured at the canopy surface at night with a LICOR line quantum sensor (LI-COR Inc., Lincoln, NE) and a 660/730 Sensor SKR 110 (Skye Instrument Ltd., Powys, UK), respectively. During the treatment imposition, lights were automatically turned on before sunset and off at the required time depending on the length of extension. To calculate photoperiod both civil twilights (the period beginning or ending when
the center of the sun is geometrically 68 below the horizon) were taken into account. 2.3. Data collection and analysis Phenological stages (Fehr and Caviness, 1977) were recorded at 1–3-day intervals in a previously defined area of three bordered rows of 0.50 m long in each subplot. The timing of a particular developmental stage was determined as the date when 50% of the plants of the monitored area reached it. Durations of R1–R3, R3–R6 and R6–R8 were computed for each subplot. At maturity, two adjacent rows of 1 m long were harvested and the number of nodes, pods and seeds were counted. The number of seeds per node was calculated at a whole plant level, relating seed number and total node number per plant. Average seed weight was estimated from three randomly taken sub-samples of 100 seeds per subplot. 2.4. Meteorological data and calculations Data of daily global solar radiation and maximum and minimum temperatures were obtained from a standard meteorological station located ca. 300 m away from the plots, estimating daily mean temperature as the average between maximum and minimum. The integral of solar radiation during the period for seed formation was calculated as the sum of daily incident global radiation between R3 and R6 stages. To separate thermal and photoperiodic effects on development, the duration of R3–R6 period was corrected using a linear three-segmented function (Piper et al., 1996) considering that the rate of development on day t [D(t)] is a function of temperature: DðtÞ ¼ 0 ðT TbÞ DðtÞ ¼ ðTo1 TbÞ DðtÞ ¼ 1 ðTm TÞ DðtÞ ¼ ðTm To2Þ DðtÞ ¼ 0
if T < Tb if Tb < T < To1 if To1 < T < To2
(1)
if To2 < T < Tm if T > Tm
where T is daily mean temperature, Tb = base temperature below which there is no development, To1 = lower optimum temperature, To2 = upper optimum temperature, and Tm = maximum temperature,
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
above which there is no development. According to Piper et al. (1996), cardinal temperatures for the subperiod R3–R5 were Tb = 2.5 8C, To1 = 25 8C, To2 = 30 8C and Tm = 55 8C. From R5 onwards, Tb was 48 8C and To1 was 28 8C. According to Eq. (1), one thermal day is equal to one calendar day when temperature is optimum and varies between zero and one outside this range. The accumulated thermal days between two stages, e.g. R3 and R6, represented the corrected duration of the phase, R3–R6. Considering that low temperatures may promote flower abortion and pod abscission, we defined an effective time for pod addition as the period thermally adequate for setting pods. It was estimated computing the accumulated thermal days between R3 and R6, using Eq. (1) with the cardinal temperatures proposed by Boote et al. (1997) for the pod addition process: Tb = 14 8C, To1 = 21.5 8C, To2 = 26.5 8C and Tm = 40 8C. To evaluate the possible joint effects of radiation and temperature on seed number, we defined the effective radiation on day t [ER(t)] as: ERðtÞ ¼ DðtÞRðtÞ
(2)
215
where D(t) is the rate of development on day t, estimated with Eq. (1) using the cardinal temperatures proposed for the pod addition process, and R(t) is the daily incident global radiation. The sum of ER(t) from R3 to R6, was defined as the effective radiation accumulated in the critical period. Each calculation was independently performed for each subplot. Results were compared with those previously obtained with the same genotypes in an independent experiment carried out a year before, in which photoperiod was extended only by 2 h in relation to natural daylength (Kantolic and Slafer, 2001).
3. Results 3.1. Development All the extended photoperiod regimes increased the duration of the R3–R6 period for both genotypes (Table 1). Both cultivars showed a quantitative type of response throughout the whole range of explored photoperiods, though the cultivar A-5409, exhibited a stronger response than that of Dekalb-CX-458.
Table 1 Duration and average temperatures of R3–R6 and R6–R8 periods of soybean grown under natural photoperiod (DNAT) or exposed to artificially extended photoperiods 1.5, 3.0, 4.5 or 6.0 h longer than natural (D+1.5 through D+6.0) between R3 stage and physiological maturity R3–R6 Duration (days) A-5409 DNAT D+1.5 D+3.0 D+4.5 D+6.0 Dekalb-CX-458 DNAT D+1.5 D+3.0 D+4.5 D+6.0 LSDa LSDb MSc photoperiod MSc cultivar MSc interaction a b c
R6–R8 Temperature (8C)
Duration (days)
Temperature (8C)
34.0 52.7 76.7 91.0 100.3
24.2 22.5 21.7 20.9 20.2
19.0 30.0 29.3 28.7 21.7
22.0 16.9 15.3 15.0 12.3
31.0 37.7 45.0 53.3 64.3
24.3 24.3 23.9 23.0 22.1
15.0 43.3 52.0 58.0 51.0
23.3 19.9 17.6 16.6 15.8
2.6 2.4 2477** 4838** 266**
0.6 0.6 17.2** 15.0** 1.4**
9.3 11.1 645** 2484** 297**
1.3 1.2 56.5** 22.4* 0.6 ns
LSD (p = 0.05) between means, within photoperiod treatments. LSD (p = 0.05) between means, between photoperiod treatments. Mean square of the analysis of variance and significance of the principal effects and interactions (**p < 0.01; *p < 0.05; ns: not significant).
216
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
As plants were grown under field conditions, the delay in reaching the R6 stage resulted in a decrease of average temperature for the R3–R6 period (Table 1). For that reason, the right estimation of photoperiod sensitivity required taking into account thermal effects on developmental rate. When relating corrected duration of R3–R6 with average photoperiod, a typical short-day response was evident for both cultivars (Fig. 1), that closely matched previous results (open symbols in Fig. 1). Although greater sensitivity of A-5409 remained evident, its sensitivity was not constant across the whole range of explored photoperiods (Fig. 1). Development responses during the R6–R8 phase resulted less noticeable and more variable. Longer durations were obtained in Dekalb-CX-458 under long photoperiods (Table 1) but the response of both cultivars was not quantitative across the whole range of explored photoperiods (Fig. 2).
photoperiod. In average, plants grown under extended photoperiod produced ca. 75% more seeds than plants grown under natural photoperiod. In Dekalb-CX-458, maximum number of seeds was produced in plants grown under the three most extended photoperiod regimes, without significant differences between them. For this cultivar, plants grown under the most extended photoperiod produced twice the number of seeds as the control plants. Exposure to extended photoperiods increased the number of nodes both in the mainstem and in the branches, with a stronger response in A-5409 (Fig. 3). In both cultivars, a slight but significant increase in the number of seeds per node was produced under extended photoperiods (Table 2).
3.2. Number of seeds
The relationship between seed number and the duration of R3–R6 was curvilinear (Fig. 4) as a result of the quantitative response in the duration of R3–R6 stage combined with the absence of differences in the number of seeds and pods produced between the most extended photoperiod regimes. To explore whether this apparent saturation in the response of seed number to the length of the R3–R6 period for the longest durations could be related, at
Exposing plants to extended photoperiod after R3 increased the number of pods and seeds, without consistent changes in seed number per pod (Table 2). In A-5409, there were no differences in pod and seed number between the four regimes of extended
Fig. 1. Relationship between the duration of the period R3–R6 corrected by temperature and mean photoperiod for A-5409 (diamonds) and Dekalb CX 458 (triangles). Open symbols correspond to previous results (Kantolic and Slafer, 2001). Vertical bars represent the standard error of the means and are shown when bigger than symbols. Duration of the R3–R6 period was corrected using cardinal temperatures proposed by Piper et al. (1996).
3.3. Relationship between the duration of the critical period and the number of seeds
Fig. 2. Relationship between the corrected duration of the period R6–R8 and mean photoperiod for A-5409 and Dekalb CX 458. Symbols as in Fig. 1. Duration of the R6–R8 period was corrected using cardinal temperatures proposed by Piper et al. (1996).
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
217
Table 2 Average number of pods and seeds per square meter and number of seeds per pod and per node, in soybean plants grown under natural photoperiod (DNAT) or exposed to artificially extended photoperiods 1.5, 3.0, 4.5 o 6.0 h longer than natural (D+1.5 through D+6.0) between R3 stage and physiological maturity Number of pods (m2)
Number of seeds (m2)
(pod1)
(node1)
A-5409 DNAT D+1.5 D+3.0 D+4.5 D+6.0
1659 2649 3189 2801 2724
3705 6346 6677 6526 6300
2.2 2.4 2.3 2.3 2.3
3.1 3.6 3.7 3.2 3.4
Dekalb CX-458 DNAT D+1.5 D+3.0 D+4.5 D+6.0
773 1323 1834 1883 1841
2102 3439 4330 4748 4895
2.6 2.4 2.4 2.5 2.7
2.3 3.1 3.2 3.5 3.8
646 658 1575418** 8644755** 126303 ns
1619 1143 8066973** 30236464** 563986 ns
0.1 0.2 0.01 ns 0.47** 0.03*
0.5 0.6 0.758** 0.367 ns 0.423 ns
LSD 1a LSD 2b MSc photoperiod MS cultivar MS interaction a b c
Least significant difference (p = 0.05) between means, within photoperiod treatments. Least significant difference (p = 0.05) between means, between photoperiod treatments. Mean square of the analysis of variance and significance of the principal effects and interactions (**p < 0.01; *p < 0.05; ns: not significant).
least partly, to environmental limitations, we analyzed how long increments in R3–R6 duration really implied more time to grow and set pods. Due to the fact that temperatures and radiation steadily decreased as the
season progressed, the longest durations of R3–R6 did not represent important increments in radiation capture nor did they extend the effective time for pod addition (Fig. 5).
Fig. 3. Number of nodes in mainstem (solid bars) and in branches (open bars) in soybean plants grown under natural or artificially extended photoperiods. Under each bar, the hours of extension of photoperiod applied is shown. Vertical lines show the standard error of the means.
Fig. 4. Relationship between the number of seeds per square meter and the duration of the R3–R6 period for A-5409 and Dekalb CX 458. Symbols as in Fig. 1.
218
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
seed weight, when occurred, were far smaller than increases in number of seeds per unit land area.
4. Discussion
Fig. 5. Relationship between the increments in the effective time for pod addition (closed symbols) and in accumulated radiation (open symbols) during R3–R6 and the increments in duration of this phase produced by photoperiod extensions, for A-5409 (diamonds) and Dekalb CX458 (triangles). Increments are expressed in relative terms to the environmental conditions explored in the plants exposed to natural photoperiod. The effective time for pod addition was estimated according to the cardinal temperature proposed by Boote et al. (1997) for the pod addition process, as explained in the text. The dotted line represents the 1:1 relationship.
3.4. Seed weight Average seed weight tended to be reduced in plants exposed to extended photoperiod and the magnitude of these effects depended both on cultivars and photoperiod regimes. Extending photoperiod in 1.5 h slightly reduced seed weight only in A-5409 while the longest extension reduced seed weight by ca. 20% in both cultivars (Fig. 6). In any case, reductions in
Fig. 6. Average seed weight of soybean plants exposed to different photoperiods from R3 to maturity. Vertical lines show the standard error of the means.
Photoperiod modified the duration of the critical period for seed determination in both indeterminate soybean cultivars and this response was evident over a wide range of photoperiods. Photoperiodic effects during post-flowering phases have been previously reported (Thomas and Raper, 1976; Guiamet and Nakayama, 1984a,b; Morandi et al., 1990; Summerfield et al., 1998; Ellis et al., 2000; Kantolic and Slafer, 2001). The results of the present study showed that this response is quantitative even at photoperiods longer than those generally explored by soybean crops grown commercially. Cultivar A-5409 expressed a greater sensitivity to photoperiod during reproductive period than Dekalb-CX-458, confirming initial results from which these cultivars were selected for this study (Kantolic and Slafer, 2001). Plants exposed to longer photoperiods produced more nodes although the extension of daylength began, in average, as late as 18 days after first flowering. The terminal apex of indeterminate soybeans may become reproductive even after R1 stage (Caffaro et al., 1988) so that the increased node number in response to extended photoperiod may reflect that the apex was still able to respond to changes in daylength even after the R3 stage. Moreover, long photoperiods have been found to promote the elongation of internodes and dry matter partitioning towards vegetative organs, thus allowing more growth of the differentiated internodes (Caffaro et al., 1988). Photoperiodic effects on branch growth have been previously reported (Board and Settimi, 1986; Caffaro and Nakayama, 1988; Kantolic and Slafer, 2001), although it remains unclear whether the increased number of branch nodes was a result of a development effect (i.e. more days were available for internodes to be differentiated and elongated) or a consequence of more growth due to a longer period intercepting radiation (more carbohydrates were available for vegetative organs to grow). In the present study, the increment in node number was evident only between plants from natural and extended photoperiods, while there was no difference between the four extended photoperiod regimes. These findings contrast with the
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
quantitative response in the developmental rate. Although our study was not designed to investigate photoperiodic control of node number, the absence of a quantitative response suggests that other factors, besides those controlling node differentiation, may be involved in determining the final number of nodes. Minor changes occurred in seed number per pod in response to photoperiod extension, in coincidence with previous results (Kantolic and Slafer, 2001). Similar findings of small or no significant changes in seed number per pod have been reported in studies that manipulated incident radiation (Schou et al., 1978; Mathew et al., 2000), plant population (Dominguez and Hume, 1978) or canopy architecture (Board et al., 1996), confirming the remarkably high stability of this yield component and its minor importance in defining seed number per unit land area and yield across environments. Increased node fertility, expressed as seed number per node in response to extended photoperiod, was therefore a consequence of an increase in pod number per node. This has been also found in our previous study (Kantolic and Slafer, 2001) and several papers highlighted the relevance of this yield component in determining soybean yield (e.g. Board et al., 1999; Ball et al., 2001). Pod number per node is the result of the balance between the generation and the mortality of flowers and pods. The generation of pods includes the initiation of flower buds and their development into mature flowers. Both processes are affected by photoperiod (Thomas and Kanchanapoom, 1991; Zhang et al., 2001). However, the production of more flowers does not warrant an increase in the number of pods, as enlarging pods can fail to set (Westgate and Peterson, 1993). Both the production and the abortion of mature flowers and young pods are sensitive to changes in photosynthate supply during flowering and pod set (Jiang and Egli, 1993; Bruening and Egli, 1999, 2000). This means that if exposure to extended photoperiod could enhance seed number per node, its effects should somehow improve the balance between source strength and sink demand, preventing abortion. The relationship between seed number and the duration of R3–R6 was curvilinear, suggesting some kind of saturation of the response at durations longer than a threshold. However, because of the delay in development itself produced by the longest daylengths, further lengthening the R3–R6 phase beyond that
219
threshold did not represent actual increases in the radiation available for growth nor in the time thermally effective to set pods. Pod addition is highly sensitive to low temperatures (Thomas and Raper, 1976; Hume and Jackson, 1981) while low radiation reduces pod number through reductions of crop growth rate (Board et al., 1992). This means that the improving of seed number by increasing the duration of R3–R6 through photoperiod, should be conditioned to a concomitant improvement in crop growth and partitioning to pods. Rearranging our results and relating seed number with the radiation accumulated during R3–R6 (Fig. 7a) or with the duration of R3–R6 corrected by temperature (Fig. 7b), reduced the curvilinearity evidenced in A-5409 when seed number was related to duration of R3–R6 (Fig. 4). When both thermal and radiation conditions were jointly taken into account by estimating the effective radiation for the R3–R6 period, the differences between treatments of extended photoperiod disappeared and the relationship became mostly linear (Fig. 7c). This linearity, compared with the curvilinear relationship when using duration as the independent variable, suggests that even though more days elapsed to complete the R3–R6 phase under the longest photoperiods, this latter lengthening of the critical phase did not imply differences in conditions for pod growth. In the present study, average seed weight was reduced in the treatments of extended photoperiod, mainly in A-5409. Exposure to long photoperiods has been found to reduce seed growth rate and final seed weight in controlled environments (Raper and Thomas, 1978; Morandi et al., 1988). However, other causes beyond direct photoperiod effects may be involved in this study. As the length of R3–R6 increased by photoperiodic effects, the seed growth period was delayed into worse environmental conditions (lower temperature and lower radiation). Low temperatures reduce seed growth rate (Egli, 1998) and the average temperature was lower during the seedfilling period of plants exposed to longer photoperiods from R3 onwards. It is known that seed growth is usually limited by assimilate supply (Egli, 1999), though it seems to be a large variability in the degree of source limitation for seed filling in soybean (Borra´ s et al., 2004). In the preset study, comparing the extreme treatments, seed size was reduced by ca. 20% while seed number was increased by more than 75%. Thus, if a competitive relationship was established
220
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
Fig. 7. Relationship between: the number of seeds and (i) accumulated solar radiation between R3 and R6 stages (a); (ii) the duration of R3–R6 corrected by thermal conditions for pod addition equations (b); and (iii) radiation powered by thermal conditions (effective radiation, panel c). Symbols as in Fig. 1. Temperature coefficients for correcting the duration of R3–R6 and powering radiation were taken from Boote et al. (1997).
between the growing seeds during the seed-filling phase, it was not mutually exclusive, and yield was undoubtedly improved by exposing plants to longer photoperiod after R3. It must be noted, however, that probable applications of our finding include genetic manipulation of crop sensitivity to photoperiod, developing cultivars that flower earlier and extend the post-flowering period (Kantolic and Slafer, 2001), thus seed filling should not occur under unfavorable
conditions. In this context, emphasis should be put on improving the understanding of photoperiodic effects on pod and seed number. The fact that seed number increased under long photoperiods only when more radiation was available and that the relationship between the number of seeds and their average size was not completely competitive, reinforce the hypothesis that photoperiod effects on seed number should include mechanisms related with carbon metabolism. Although the nature of the mechanisms remains unclear, they should include any or both of the regulation components of pod and seed set (Egli and Bruening, 2002a): the supply of assimilates from photosynthesis and the utilization of assimilates by the seeds. In this study, it can be assumed that the daily supply of assimilates has been maximized, as maximum interception of radiation was achieved at the beginning of the reproductive period and stresses were avoided. However, we cannot discard possible effects of the treatments on the distribution of assimilates within the plants. One critical aspect of assimilate utilization seems to be the simultaneous growth of pods of widely different ages, as the rapid growth of older pods may reduce assimilate supply to flowers and young pods, triggering their abortion (Egli and Bruening, 2002b). Although photoperiod is known to modify the dynamics of flower production and pod growth under controlled environment (Guiamet and Nakayama, 1984a; Morandi et al., 1990), it is not clear if this mechanism may be underlying the responses observed in the current investigation. Evidently, more research in intact plants grown in the field is needed to clarify whether photoperiod increases seed number through increasing assimilate availability (as a longer R3–R6 period may result in greater total radiation interception and greater production of assimilates) or also by reducing instantaneous sink demand, by modifying timing of flowers and pod production. Experiments consisting of the factorial combination of photoperiod extensions and shading in field plots may help solve this issue.
Acknowledgements We gratefully acknowledge the support given by competitive grants from both Agencia Nacional de
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
Promocion Cientifica y Tecnologica (FONCyT program) and Universidad de Buenos Aires (UBACyT program). GAS was working at the Universidad de Buenos Aires and CONICET during the experimental growing seasons and at ICREA/Universitat de Lleida during final analysis of results and writing of the ms.
References Ball, R.A., McNew, R.W., Vories, E.D., Keisling, T.C., Purcell, L.C., 2001. Path analyses of population density effects on short-season soybean yield. Agron. J. 3, 187–195. Board, J.E., Settimi, J.R., 1986. Photoperiod effect before and after flowering on branch development in determinate soybean. Agron. J. 78, 995–1002. Board, J.E., Tan, Q., 1995. Assimilatory capacity effects on soybean yield components and pod number. Crop Sci. 35, 846–851. Board, J.E., Kamal, M., Harville, B.G., 1992. Temporal importance of greater light interception to increased yield in narrow-row soybean. Agron. J. 84, 575–579. Board, J.E., Zhang, W., Harville, B.G., 1996. Yield rankings for soybean cultivars grown in narrow and wide rows with late planting dates. Agron. J. 88, 240–245. Board, J.E., Kang, M.S., Harville, B.G., 1999. Path analyses of the yield formation process for late-planted soybean. Agron. J. 91, 128–135. Boote, K.J., Jones, J.W., Hoogenboom, G., 1997. Simulation of crop growth: CROPGRO model. In: Peart, R.M., Curry, R.B. (Eds.), Agricultural Systems Modeling. Marcel Dekker, NY, pp. 651– 692. Borra´ s, L., Slafer, G.A., Otegui, M., 2004. Seed dry weight response to source-sink manipulations in wheat, maize and soybean: a quantitative reappraisal. Field Crops Res. 86, 131–146. Bruening, W.P., Egli, D.B., 1999. Relationship between photosynthesis and seed number at phloem isolated nodes in soybean. Crop Sci. 39, 1769–1775. Bruening, W.P., Egli, D.B., 2000. Leaf starch accumulation and seed set at phloem- isolated nodes in soybean. Field Crops Res. 68, 113–120. Caffaro, S.V., Nakayama, F., 1988. Vegetative activity of the main stem terminal bud under photoperiod and flower removal treatments in soybean. Aust. J. Plant Physiol. 15, 475–480. Caffaro, S.V., Martignone, R.A., Torres, R., Nakayama, F., 1988. Photoperiod regulation of vegetative growth and meristem behavior toward flower initiation of an indeterminate soybean. Bot. Gaz. 149, 311–316. Calvin˜ o, P.A., Sadras, V.O., Andrade, F.H., 2003. Development, growth and yield of late-sown soybeans in the southern Pampas. Eur. J. Agron. 19, 265–275. Dominguez, C., Hume, D.J., 1978. Flowering, abortion and yield of early maturing soybeans at three densities. Agron. J. 70, 801– 805. Egli, D.B., 1997. Cultivar maturity and response of soybean to shade stress during seed filling. Field Crops Res. 52, 1–8.
221
Egli, D.B., 1998. Seed Biology and the Yield of Grain Crops. CAB International, UK. Egli, D.B., 1999. Variation in leaf starch and sink limitations during seed filling in soybean. Crop Sci. 39, 1361–1368. Egli, D.B., Zhen-wen, Y., 1991. Crop growth rate and seeds per unit area in soybeans. Crop Sci. 31, 439–442. Egli, D.B., Bruening, W.P., 2000. Potential of early-maturing soybean cultivars in late plantings. Agron. J. 92, 532–537. Egli, D.B., Bruening, W.P., 2002a. Synchronous flowering and fruit set at phloem-isolated nodes in soybean. Crop Sci. 42, 1535– 1540. Egli, D.B., Bruening, W.P., 2002b. Flowering and fruit set dynamics at phloem-isolated nodes in soybean. Field Crops Res. 79, 9–19. Ellis, R.H., Asumadu, H., Qi, A., Summerfield, R.J., 2000. Effects of photoperiod and maturity genes on plant growth, partitioning, radiation use efficiency and yield in soyabean [Glycine max (L.) Merrill] ‘Clark’. Ann. Botany 85, 335–343. Farquhar, G.D., Sharkey, T.D., 1994. Photosynthesis and carbon assimilation. In: Boote, K.J., Bennet, J.M., Sinclair, T.R., Paulsen, G.M. (Eds.), Physiology and Determination of Crop Yield. ASA CSSA SSSA, Madison, WI, pp. 187–210. Fehr, W.R., Caviness, C.E., 1977. Stages of soybean development. Spec. Rep. 80, Iowa State University, Ames, Iowa. Grimm, S.S., Jones, J.W., Boote, K.J., Herzog, D.C., 1994. Modeling the occurrence of reproductive stages after flowering for four soybean cultivars. Agron. J. 86, 31–38. Guiamet, J.J., Nakayama, F., 1984a. The effects of long days upon reproductive growth in soybeans (Glycine max (L.) Merr.) cv. Williams. Jpn. J. Crop Sci. 53, 35–40. Guiamet, J.J., Nakayama, F., 1984b. Varietal responses of soybeans (Glycine max (L.) Merr.) to long days during reproductive growth. Jpn. J. Crop Sci. 53, 299–306. Herbert, S.J., Litchfield, G.V., 1982. Partitioning soybean seed yield components. Crop Sci. 22, 1074–1079. Hume, D.J., Jackson, A.K.H., 1981. Pod formation in soybeans at low temperature. Crop Sci. 21, 933–937. Jiang, H., Egli, D.B., 1993. Shade induced changes in flower and pod number and flower and fruit abscission in soybean. Agron. J. 85, 221–225. Jiang, H., Egli, D.B., 1995. Soybean seed number and crop growth rate during flowering. Agron. J. 87, 264–267. Kantolic, A.G., Slafer, G.A., 2001. Photoperiod sensitivity after flowering and seed number determination in indeterminate soybean cultivars. Field Crops Res. 72, 109–118. Liu, F., Jensen, C.R., Anderson, M.N., 2004. Drought stress effect on carbohydrate concentration in soybean leaves and pods during early reproductive development: its implication in altering pod set. Field Crops Res. 86, 1–13. Mathew, J.P., Herbert, S.J., Zhang, S., Rautenkranz, A.A.F., Litchfield, G.V., 2000. Differential response of soybean yield components to the timing of light enrichment. Agron. J. 92, 1156– 1161. Morandi, E.N., Casano, L.M., Reggiardo, L.M., 1988. Post-flowering photoperiodic effect on reproductive efficiency and seed growth in soybean. Field Crops Res. 18, 227–241. Morandi, E.N., Schussler, J.R., Brenner, M.L., 1990. Photoperiodically induced changes in seed growth rate of soybean as related
222
A.G. Kantolic, G.A. Slafer / Field Crops Research 93 (2005) 212–222
to endogenous concentrations of ABA and sucrose in seed tissues. Ann. Bot. 66, 605–611. Piper, E., Boote, K.J., Jones, J.W., Grimm, S.S., 1996. Comparison of two phenology models for predicting flowering and maturity date of soybean. Crop Sci. 36, 1606–1614. Raper, C.D., Thomas, J.F., 1978. Photoperiodic alteration of dry matter partitioning and seed yield in soybeans. Crop Sci. 18, 654–656. Raper, C.D., Kramer, P.J., 1987. Stress physiology. In: Wilcox, J.R. (Ed.), Soybeans: Improvement, Production and Uses. second ed. ASA CSSA SSA, Madison, WI, agronomy monograph no. 16, pp. 589–641. Schou, J.B., Jeffers, D.L., Streeter, J.G., 1978. Effects of reflectors, black boards, or shades applied at different stages of plant development on yield of soybeans. Crop Sci. 18, 29–34. Summerfield, R.J., Asumadu, H., Ellis, R.H., Qi, A., 1998. Characterization of the photoperiodic response of post-flowering
development in maturity isolines of soyabean [Glycine max (L.) Merrill] ‘Clark’. Ann. Botany 82, 765–771. Thomas, J.F., Raper Jr., C.D., 1976. Photoperiodic control of seed filling for soybeans. Crop Sci. 16, 667–672. Thomas, J.F., Kanchanapoom, M.L., 1991. Shoot meristem activity during floral transition in Glycine max (L.) Merr. Bot. Gaz. 152, 139–147. Washburn, C.F., Thomas, J.F., 2000. Reversion of flowering in Glycine max (Fabaceae). Am. J. Bot. 87, 1425–1438. Westgate, M.E., Peterson, C.M., 1993. Flower and pod development in water-deficient soybeans (Glycine max L. Merr). J. Exp. Bot. 44, 109–117. Zhang, L., Wang, R., Hesketh, J.D., 2001. Effects of photoperiod on growth and development of soybean floral bud in different maturity. Agron. J. 63, 944–948.