Physiological activity and biomass production in crop canopy under a tropical environment in soybean cultivars with temperate and tropical origins

Field Crops Research 216 (2018) 209–216

Contents lists available at ScienceDirect

Field Crops Research journal homepage: www.elsevier.com/locate/fcr

Physiological activity and biomass production in crop canopy under a tropical environment in soybean cultivars with temperate and tropical origins

T

⁎

Andy Saryokoa,b, , Yasuko Fukudaa, Iskandar Lubisc, Koki Hommad, Tatsuhiko Shiraiwaa a

Laboratory of Crop Science, Graduate School of Agriculture, Kyoto University, Japan Indonesian Agency for Agricultural Research and Development (IAARD), Ministry of Agriculture, Indonesia c Department of Agronomy and Horticulture, Faculty of Agriculture, Bogor Agriculture University, Indonesia d Laboratory of Crop Science, Graduate School of Agriculture Science, Tohoku University, Japan b

A R T I C L E I N F O

A B S T R A C T

Keywords: Canopy temperature Soybean Transpiration Tropical environment

In order to explore the plant factors facilitating better adaptation of soybean to high temperatures, genotypic variability till the beginning of seed filling (R5) were examined with reference to biomass production, relative transpiration activity and relevant plant factors under a tropical environment. Twenty-nine (in 2014 and 2015) and 20 (in 2016) soybean cultivars of temperate (Japan and USA) and tropical (Indonesia-old, Indonesiamodern, and Others) origin were grown in Serang, Banten (2014 and 2015; Experiment 1) and in Bogor, West Java (2016; Experiment 2), Indonesia. In Experiment 1, aboveground biomass at R5 (TDWR5) of the temperate cultivars was one-third to one-fourth of that of the tropical cultivars. This was associated with less than half the amount of the cumulative intercepted radiation to R5 (CIRR5) due to their shorter growth duration and lower value of the mean fraction of canopy light interception till R5 (mean FVE-R5). In addition, the radiation use efficiency (RUE) at R5 of the temperate cultivars was also as low as 0.54 g MJ−1, as compared to 0.87 g MJ−1 in the tropical cultivars. The value of canopy temperature minus air temperature (CTd), as an indicator of relative transpiration activity, of temperate cultivars was markedly larger than that of the tropical cultivars, indicating lower transpiration activity in temperate cultivars, which was associated with the low RUE. In Experiment 2, greater activity of transpiration in tropical cultivars was attributed to their higher stomatal conductance (gs) and greater stomatal density (Nstoma) of upper leaves than that in those from the temperate regions. These results indicate that low biomass production in temperate cultivars occurs not only due to the cumulative intercepted radiation in the canopy but also due to low RUE and that the low RUE in temperate cultivars is associated with low gas exchange activity, in which leaf morphological traits are involved. Within temperate cultivars, US cultivars tended to perform better than the Japanese cultivars with respect to gas exchange activity.

1. Introduction Soybean [Glycine max (L.) Merr.] is one of the most important crops globally, and is used often as protein meal and vegetable oil. Worldwide, the total area supporting soybean production has expanded more rapidly than that of any other major crop since the 1970s, increasing from 29.5 million ha in 1970–117.5 million ha in 2014 (Food and Agriculture Organization, 2017), in response to growing global demand for soybean products over the past four decades. Soybean production is largely predominant in temperate regions due to cool to

moderately warm climates, with the USA, Brazil, and Argentina accounting for 84% of the world’s harvest in 2014. Expanding soybean production to the tropical regions represents a possible means for increasing global soybean production in order to meet soaring consumer demand; soybean cultivation in the warmer and wetter climates of the tropics represent numerous challenges, however. Soybean production in relatively high-temperature environments has also increased throughout temperate regions due to climate change and global warming, and increasing of global surface temperatures will have significant impacts on soybean production (Prasad et al., 2006), especially

Abbreviations: CIRR5, cumulative intercepted radiation to R5; CTd, canopy temperature minus air temperature; F, fraction of radiation intercepted; FVE-4WAP, F from seedling emergence to four weeks after planting; FVE-R5, F from seedling emergence to R5; gs, stomatal conductance; Lguard, guard cell length; Lvein, total leaf venation; Nepi, epidermal cell density; Nstoma, stomatal density; RUE, radiation use efficiency; SI, stomatal index; TDWR5, aboveground biomass at R5; Δ, carbon isotope discrimination ⁎ Corresponding author at: Laboratory of Crop Science, Graduate School of Agriculture, Kyoto University, Sakyo, Kyoto 606-6042, Japan. E-mail addresses: [email protected], [email protected] (A. Saryoko). https://doi.org/10.1016/j.fcr.2017.11.012 Received 21 August 2017; Received in revised form 13 November 2017; Accepted 13 November 2017 0378-4290/ © 2017 Elsevier B.V. All rights reserved.

Field Crops Research 216 (2018) 209–216

A. Saryoko et al.

in those tropical regions where current climatic conditions and temperatures are close to optimum for soybean growth, for which further temperature increase will reduce yields (Prasad et al., 2017). The effects of higher ambient temperatures on soybean have been studied extensively under both, field and controlled laboratory conditions, and indirectly through the construction of model simulations (Tacarindua et al., 2012, 2013; Kumagai and Sameshima, 2014; Kantolic et al., 2013; Kantolic and Slafer, 2001; Wu et al., 2015; Setiyono et al., 2007, 2010). Tacarindua et al. (2012, 2013), for instance demonstrated that elevated temperature had a significant negative effect on soybean performance in a temperature gradient chamber (TGC), with slower growth rate resulting in reduced yield and biomass. Moreover, it has been shown that higher temperatures alter plant phenology and hasten flowering onset (Han et al., 2006; Wu et al., 2015; Kantolic and Slafer, 2005, 2007; Setiyono et al., 2007, 2010; Gaynor et al., 2011), enhance plant development (Craufurd and Wheeler, 2009), and in some cases, prolong the seed filling period (Tacarindua et al., 2013; Thomas et al., 2010). High temperatures effect on soybean also result in smaller seed size (Tacarindua et al., 2013; Thomas et al., 2010), increase seed shriveling (Tacarindua et al., 2013; Thomas et al., 2010; Smith et al., 2008; Bellaloui et al., 2017), and reduce nutritional quality (Smith et al., 2008; Bellaloui et al., 2017) and seed germination and vigor (Chebrolu et al., 2016; Smith et al., 2008; Bellaloui et al., 2017). Although the effects of temperature on yield and growth performance of soybean are well documented, less is known about the role of genetic variability in soybean responsiveness to high temperature (Mochizuki et al., 2005; Chebrolu et al., 2016) and, whether cultivars adapted to temperate and tropical regions differ in their adaptation to warm climates. Tropical environments are characterized by relatively warm temperatures and constant day-length (time from sunrise to sunset) throughout the year. Monthly mean air temperatures in the tropics range between 20 and 30 °C and the difference in mean temperatures between cool and hot months is typically less than 7 °C (Monteith, 1977). In the tropics, the day-length is just over 12 h at the equator as against 10.6–13.7 h at 25° latitude. Such environmental conditions are typical in Indonesia, thus making the country an ideal location for studying the growth, development, and physiological aspects of soybean for adaptation to future climate change. In a previous study, we had shown that the yield and seed quality of temperate cultivars grown in tropical environments were lower than those of tropical cultivars even after differences in growth duration were taken into account (Saryoko et al., 2017). We also found that harvest index between the temperate and the tropical groups did not differ considerably, indicating that the process of biomass production may be involved in these differences. The objective of the present study was to assess the role of genotypic variability among soybean cultivars originating from temperate and tropical regions with respect to crop physiological activity and biomass production, relative transpiration activity, and its associated factors under a tropical environment.

Table 1 Name, origin and classification of regions of soybean cultivars for Experiment 1 and 2. Group of origin (n)

Cultivar name

region

Japan (n = 5)

Enrei, PI416937, Tanbaguro, Tachinagaha and Fukuyutaka UA4805, DS24-2, DS25-1, DS34-3 and DS65-4 Merapi, Tidar, Ringgit, Wilis and Local Tegineneng Dering-1, M100-47-52-13†), M150-7B-41-10†), Tanggamus and SC-1-8†)

Temperate

USA (n = 5) Indonesia-old (n = 5) Indonesia-modern (n = 5 or n = 2) Other tropical (n = 9 or n = 3)

MANSHUU MASSHOKUTOU†), ICHIGUUHOU†), N 2491, M 652†), SAN SAI†), SJ4, SANDEK SIENG, E C 112828†) and MISS 33 DIXI†)

Temperate Tropics Tropics

Tropics

Cultivar name followed by symbol (†) was excluded for Experiment 2.

emergence, leaving one plant per hole. Plot soils were fertilized with N (5 g m−2), P2O5 (2.7 g m−2) and K2O (7.5 g m−2) in the form of urea, calcium superphosphate, and potassium chloride, respectively. Irrigation and pest control regimes were based on regional management programs in order to optimize growth conditions. Daily air temperatures were measured with a HMP45C temperature sensor (Campbell Scientific, INC., Logan, UT), and the incident solar radiation was measured using a CMP3 pyranometer (Kipp and Zonen, B.V., The Netherlands) and recorded with a CR1000 datalogger (Campbell Scientific, Inc., Logan, UT). Plant developmental stages were recorded following the protocol described by Fehr and Caviness (1977). At the early seed filling stage (R5), six plants were collected per plot and oven dried at 80 °C for 48 h to measure the aboveground biomass (TDWR5). Canopy development was expressed as the mean value of the fraction of radiation intercepted (F). The values of F were estimated weekly from light intercepted above the canopy using a digital imaging technique (Purcell, 2000; Shiraiwa et al., 2011; Bajgain et al., 2015; Kawasaki et al., 2016), following which the daily fraction of solar radiation was estimated by interpolation and its mean was calculated. The speed of canopy development was calculated as the mean F over the period from seedling emergence until four weeks after planting (WAP, mean FVE-4WAP). Canopy size at R5 was determined as the mean F from seedling emergence to onset of R5 (mean FVE-R5). The accumulated incident solar radiation from seedling emergence to R5 was derived from daily local meteorological data. The cumulative intercepted solar radiation to R5 (CIRR5) was calculated by multiplying the mean daily incident solar radiation (SR) with the mean FVE-R5: CIRR5 (MJ m−2) = SR × mean FVE-R5

(1)

Energy utilization efficiency was estimated as radiation use efficiency (RUE) until onset of the R5 stage. The RUE was calculated as total biomass produced until the R5 stage per cumulative intercepted radiation:

2. Material and methods

RUE (g MJ

2.1. Experiment 1

−1

) = TDWR5/CIRR5

(2)

Digital images of the canopy were captured with an infrared camera (Thermo Gear G100EX, Nippon Avionics, Japan) three times daily (around 10 AM, 11:30 AM, and 1 PM) three days a week at six WAP (Supplemental 1). Infrec Analyzer software (Nippon Avionics, Japan) was used to estimate canopy temperature (CT) from the digital images. Canopy temperature minus air temperature (CTd) was calculated as the difference between CT and air temperature (AT) at the time of the measurements:

Twenty-nine soybean cultivars were grown from July–November 2014 and from March–July 2015 at the AIAT Banten Research Station in Serang, Banten Province, Indonesia (lat. 6.1°S, long. 106.2°E). The cultivars were divided into five groups based on the region of their origin, which consisted of Japan and USA (temperate cultivars), and Indonesia-old, Indonesia-modern, and Others (tropical cultivars); the cultivars are listed in Table 1. Cultivars were selected on the basis of region, maturing traits, and representativeness of commercial cultivars. Seeds were sown in 2.4 m × 2 m plots on July 19, 2014 and were arranged in a spacing of 50 × 20 cm, and on March 17, 2015 in a spacing of 40 × 20 cm, with three replicates. Plants were thinned after seedling

CTd (°C) = CT − AT

210

(3)

Field Crops Research 216 (2018) 209–216

A. Saryoko et al.

and the US cultivars were 86.9 g m−2 and 68.4 g m−2, respectively, and of the Indonesian-old, Indonesian-modern and other tropical cultivar groups were 233.3, 255.2 and 307.6 g m−2, respectively (Table 3); a similar TDWR5 pattern was evident in 2015. Moreover, the TDWR5 of the Japanese and US cultivars were significantly smaller than those of the Indonesian-old, Indonesian-modern and other tropical cultivars. The CIRR5 in the 2014 and 2015 experiments ranged from 215.3–487.6 MJ m−2 and from 234.5–508.6 MJ m−2, respectively (Table 3). There were no significant differences in CIRR5 between two years. The CIRR5 of the temperate cultivars was markedly smaller than the tropical cultivars in both years (Table 3). Averaged across the years, TDWR5 was determined to be correlated with CIRR5 (r = 0.74), RUE (r = 0.89), growth duration to R5 (r = 0.69), and mean FVE-R5 (r = 0.70) (data not shown). On average, RUE levels were higher in 2015 than in 2014, and differences were observed between the tropical and temperate cultivars. In 2014, the RUE of the Japanese and US cultivars were 0.40 and 0.39 g MJ−1, respectively, markedly lower than those of the tropical cultivars, which ranged from 0.60–0.75 g MJ−1 (Table 3); in 2015 the RUE of the Japanese and US cultivars were 0.70 and 0.66 MJ−1, respectively, whereas those of the tropical cultivars ranged from 0.98–1.17 g MJ−1. There was no significant variation across the years in growth duration from emergence to the R5 stage. Duration of the temperate cultivar growth was shorter (41.6 and 41.9 d in 2014 and 2015, respectively) than that of the tropical cultivars (59.0 and 58.3 d in 2014 and 2015, respectively) (Table 3). Canopy growth to the R5 stage (mean FVE-R5) was smaller in 2014 than in 2015; in 2014, the mean FVE-R5 of the Japanese and US cultivars were 26.6 and 22.9%, considerably lower than that of the tropical cultivars, which ranged from 36.4–38.9%. A similar pattern was observed between groups, with the mean FVE-R5 of the Japanese (35.8%) and US cultivars (36.1%), significantly smaller than those of the tropical cultivars (51.8–54.1%). We also compared the mean FVE-4WAP, which is an indicator of the speed of canopy development, between groups and years. At the early growth stage from seedling emergence to four WAP, no significant differences were detected between years and between groups in each year (Table 3), indicating that the temperate cultivars developed in the canopy at a relatively similar rate to that of the tropical cultivars. Thus, the lower FVE-R5 recorded for the temperate cultivars might be due to their shorter growth duration prior to the onset of the R5 stage. The CTd of the temperate cultivars was noticeably larger than that of the tropical cultivars in both years (Fig. 1a and b). In 2014, the CTd of the Japanese cultivars was considerably higher than that of all the tropical cultivars, but there were no significant differences between the Japanese and the US cultivars. In addition, the US cultivars exhibited a higher CTd than the Indonesian-old and Indonesian-modern cultivars in 2014 (Fig. 1a). In 2015, however, the CTd of the Japanese cultivars was only significantly larger than that of the Other tropical cultivar group (Fig. 1b). A general negative correlation was detected between RUE and CTd (r = −0.73) in both 2014 and 2015 (Fig. 2), but this was only significant for the Japanese cultivars in 2014 and 2015 (r = −0.79 and −0.79, respectively), and for the US cultivars in 2014 (r = −0.79) (Fig. 2).

2.2. Experiment 2 In order to confirm the results obtained for relative transpiration in Experiment 1, 20 cultivars (Table 1)—a representative sample of the cultivars used in Experiment 1—were grown at the Bogor Agricultural University Experimental Farm, Bogor, West Java Province, Indonesia (lat. 6.5°S, long. 106.7°E), approximately 110 km away from the location of Experiment 1. On April 16, 2016, seeds were sown in 2 m × 2 m plots in a 40 cm × 20 cm spatial arrangement with two replicates. Fertilization, irrigation, and pest control regimes followed recommended management programs for the region in order to optimize growth conditions. Relative transpiration activity was measured by recording CT at midday at 5, 6, and 7 WAP with an infrared camera, as described for Experiment 1; estimates of CTd were also derived using the procedure described in Experiment 1. Stomatal conductance (gs) was recorded from the upper most-fully expanded-matured leaf using a SC-1 leaf porometer (Decagon Device Inc., USA) at the time of CT measurement, following which, the leaves were further sampled for estimation of carbon composition and nitrogen content, following procedures described below. Values of CTd and gs were expressed as the averages of three measurements. Leaf morphological traits were measured following the method described by Tanaka and Shiraiwa (2009). In brief, stomatal density (Nstoma), epidermal cell density (Nepi), and guard cell length (Lguard) were measured in the abaxial part of the leaf using Suzuki’s Universal Micro-Printing method (SUMP, Tokyo, Japan). Two leaves from two plants per plot were taken from the upper most-fully expanded-matured leaf at six WAP to use as samples for analysis of stomatal morphology, with stomatal index (SI) defined as the ratio of Nstoma to total cell number, a sum of Nstoma and Nepi. Total leaf venation (Lvein) was determined by analyzing digital images of leaves; images were obtained by placing fresh leaves directly on a microscope slide and captured at 100-fold (10 × 10) magnification. Calculation of Lvein was performed using the segmented line tool of ImageJ (National Institute Health, USA) as described in Tanaka and Shiraiwa (2009). Leaf disks were collected using 3 mm leaf punchers from the same leaves that were used to measure gs, then oven-dried at 60 °C for 12 h. Carbon isotope composition was determined via comparison against a Pee Dee Belemnite (PDB) standard (δp, 13C/12C), and nitrogen content (Ncont) was estimated following the protocol described by Fukuda et al., 2017 (submitted) using a mass spectrometer (EA ConFlo IV and Delta V Advantage, ThemoFisher Scientific, USA) and expressed as mg per unit leaf weight (mg g−1). The carbon isotope discrimination (Δ) was calculated via Eq. (4) (Farquhar et al., 1982, 1989), assuming that carbon isotope composition of the air against a PDB standard (δa) was −8‰. Δ = (δa − δp)/(1 + δa/1000)

(4)

3. Results Average daily temperatures during the growth period were 27.7, 27.9 and 27.9 °C for Experiment 1 (in 2014 and 2015) and Experiment 2, respectively (Table 2). Mean minimum and maximum temperature ranged between 23.0–23.5 °C and 32.2–32.5 °C, respectively. In Experiment 1, the SR was approximately 10% lower (17.7 MJ m−2 day−1) in 2015 than in 2014 (19.5 MJ m−2 day−1). Day-length ranged between 11.8–12.0 h during all experimental periods.

3.2. Experiment 2 Comparison of the CTds of the temperate and tropical cultivars (Fig. 1c) revealed that, as in Experiment 1, the CTd of the temperate cultivars was significantly larger than that of the tropical cultivars (Fig. 2, Table 3). The average gs of the Japanese cultivars was significantly lower than that of all of the tropical cultivar groups, but not the US cultivars (Fig. 3); in general, soybean cultivars from temperate regions had significantly lower gs than those from tropical regions. Variation in leaf

3.1. Experiment 1 On average, the TDWR5 levels of both temperate and tropical cultivars were higher in 2015 than in 2014 (Table 3). The temperate cultivars consistently exhibited lower levels of TDWR5 than did tropical cultivars in both 2014 and 2015; in 2014, the TDWR5 of the Japanese 211

Field Crops Research 216 (2018) 209–216

A. Saryoko et al.

Table 2 Mean daily air temperature (T), daily incident solar radiation (SR) and precipitation during the growing period of Experiment 1 and 2. Site/Year/Experiment

Month

T (°C) Min.

Max.

Avg.

SR (MJ m−2 day−1)

Precipitation (mm)

Serang-Banten, 2014, Experiment 1

Jul. Aug. Sep. Oct. Nov. Mean

22.9 22.8 22.2 22.8 24.2 23.0

32.4 31.4 31.4 33.5 33.6 32.5

27.7 27.1 26.8 28.1 28.9 27.7

17.5 20.1 20.8 19.6 19.5 19.5

232.4 9.6 21.8 21.0 160.3 89.0

Serang-Banten, 2015, Experiment 1

Mar. Apr. May Jun. Jul. Mean

23.5 24.1 24.0 23.7 21.2 23.3

33.4 32.1 31.8 32.3 32.5 32.4

28.5 28.1 27.9 28.0 26.9 27.9

19.0 16.2 17.5 16.8 17.4 17.4

193.1 130.2 39.1 83.4 4.7 90.1

Bogor-West Java, 2016, Experiment 2

Mar. Apr. May Jun. Jul. Mean

23.7 24.0 24.1 23.0 22.7 23.5

32.0 32.7 32.6 31.9 32.0 32.2

27.8 28.4 28.3 27.5 27.3 27.9

16.8 15.5 16.3 15.2 15.1 15.8

450.0 555.0 329.7 373.1 292.5 400.1

1368 mm−2, respectively). No differences were observed in SI across the cultivar groups, with SI of cultivars from temperate and tropical regions averaging 19.1 and 19.7%, respectively. The Nstoma × Lguard of cultivars from tropical regions (5.89 mm mm−2) was significantly higher than that of temperate cultivars (5.22 mm mm−2), but no significant differences were detected between the groups. Tropical cultivars had significantly longer total venation than temperate cultivars as well; Japanese and US cultivars exhibited the shortest in Lvein (lengths of 5.13 and 5.03 mm mm−2, respectively) followed by Other tropical cultivars, Indonesian-old cultivars, and Indonesian-modern cultivars (5.63, 6.06 and 6.39 mm mm−2, respectively). CTd and gs were tightly but negatively correlated (r = −0.616)

morphological traits between the groups was also evident (Table 4), as the Nstoma of the cultivars from the temperate regions was lower (287 mm−2) than those from the tropical regions (335 mm−2), but no significant differences were found among cultivars within regional groups of origin (Table 4). The Nstoma of Japanese and US cultivars (279 and 293 mm−2, respectively) tended to be lower than that of the Indonesian-old, Indonesian-modern and other tropical cultivars by 321–337 mm−2. In contrast, the Lguard was significantly longer in temperate cultivars (18.2 μm) than in tropical cultivars (17.9 μm). Variations in Nepi were observed between the groups, with Japanese and US cultivars (1209 and 1202 mm−2, respectively) having smaller Nepi values than Indonesian-old and other tropical cultivars (1379 and

Table 3 Components of total dry weight at R5 (TDWR5), and canopy development of Experiment 1. Year/Cultivar Group 2014 Origin Japan (n = 5) USA (n = 5) Indonesia-old (n = 5) Indonesia-new (n = 5) Others tropical (n = 9) Region Temperate (n = 10) Tropical (n = 19) 2015 Origin Japan (n = 5) USA (n = 5) Indonesia-old (n = 5) Indonesia-new (n = 5) Others tropical (n = 9) Region Temperate (n = 10) Tropical (n = 19) ANOVA† Year Origin Region Year x Origin

TDWR5 (g m−2)

CIRR5 (MJ m−2)

RUE (g MJ−1)

Growth Duration (days)

Mean FVE-R5 (%)

Mean FVE-4WAP (%)

86.9b 68.4b 233.3a 255.2a 307.6a

215.3b 234.3b 425.7a 421.2a 487.6a

0.40b 0.39b 0.68a 0.60ab 0.75a

41.8b 40.8b 57.0a 56.1a 61.7a

26.6b 22.9b 37.4a 36.4a 38.9a

17.9 14.9 17.8 14.5 15.1

77.7B 274.3A

224.8B 453.8A

0.39B 0.69A

41.3B 59.0A

24.7B 37.9A

16.4 15.6

159.6b 147.9b 528.7a 455.3a 615.8a

234.5b 221.7b 510.9a 458.2a 508.6a

0.70bc 0.66c 1.04a 0.98ab 1.17a

41.6b 42.1b 59.1a 55.6a 58.9a

35.8b 36.1b 54.1a 51.8a 53.5a

18.0 16.0 15.9 16.3 15.3

153.7B 550.6A

228.1B 495.9A

0.68B 1.09A

41.9B 58.3A

35.9B 53.2A

17.0 15.8

** ** ** ns

ns ** ** ns

** ** ** ns

ns ** ** ns

** ** ** ns

ns * ns ns

CIRR5, cumulative intercepted radiation till R5; RUE, radiation use efficiency; mean FVE-R5, mean fraction of canopy light interception from emergence to R5; mean FVE-4WAP, mean fraction of canopy light interception from emergence to 4 WAP; SR, mean daily incident solar radiation. Values followed by the same letters in each column in the respective years are not significantly different as determined by Tukey’s test at the 5% level. †ANOVA for 2-yrs data; ANOVA results: ** P < 0.01; * P < 0.05; ns, not significant.

212

Field Crops Research 216 (2018) 209–216

A. Saryoko et al.

Fig. 2. RUE at R5 stage in relation to CTd of temperate and tropical cultivars. Lines are linear regressions for each cultivar groups in Experiment 1. Boxes with dashed line indicate distribution of cultivar performance in each year. Lines indicate regression lines for cultivar groups or for all cultivars for both years. Symbols were given only cultivars with high and poor performances. High performance cultivars were: EC, EC112828; Wl, Wilis; Tg, Tanggamus; and low performance cultivars were: En, Enrei; and Tc, Tachinagaha. The 14 and 15 behind the cultivar name indicate 2014 and 2015, respectively. Inserted figure is CTd performance in Experiment 2 of Tg, Wl, En and Tc. NA, data not available.

Fig. 3. Stomatal conductance (gs) of temperate and tropical cultivar groups Experiment 2. Upper, middle and lower line in the boxes are Q1, median and Q3, respectively. Boxes indicate with the same letters are not significantly different as determined by Tukey’s test at the 5% level. Bars represent the standard error of two to five cultivars within groups. **p < 0.01; *p < 0.05.

4. Discussion Fig. 1. Canopy minus air temperature difference (CTd) of temperate and tropical cultivar groups (a) Experiment 1 2014, (b) Experiment 1 2015 and (c) Experiment 2 (avg. three measurements). Upper, middle and lower line in the boxes are Q1, median and Q3, respectively. Symbol inside the box is group mean value for each group. Boxes indicate with the same letters are not significantly different as determined by Tukey’s test at the 5% level. Bars represent the standard error of two to nine cultivars within groups. **p < 0.01; *p < 0.05; ns, not significant.

Ambient temperature is relatively stable in tropical environments, and only small differences were observed between seasons and experimental years. The mean daily temperature at our experimental site ranged from 27.7–27.9 °C, which is considerably warmer than the average temperatures in the regions in which the temperate cultivars are originated. For instance, at Kyoto, Japan (35°01′N), the favorable period for soybean production is from June to October, during which the mean daily temperature is 24.0 °C (30 y average) (Japan Meteorological Agency, 2017), with high temperatures occurring only briefly in mid-summer. In this study, both early and late maturing cultivars of temperate and tropical origin were all subjected to relatively high temperatures for the entirety of the growing season. Several high-yield cultivars from various regions (e.g. Enrei and Tachinagaha from Japan; Wilis and Tanggamus from Indonesia; SJ4 and EC112828 from Other tropical locations; the heat-tolerant cultivar DS25-1 from the US (USDA-ARS, 2017)) were included in this study. Although those cultivars are well suited to the conditions prevalent in their regions of origin, the temperate cultivars performed relatively

(Table 5), and a strong correlation was also detected between gs and Nstoma (r = 0.597); in addition, CTd was negatively correlated with Nstoma (r = −0.453). No significant differences were found in the means of Δ between groups of origin (Fig. 4a), but mean Ncont was significantly higher in tropical cultivars than cultivars from temperate regions (Fig. 4b). On average, Ncont of the Japanese and US cultivars were lower than the Indonesian-modern cultivars, but not significantly different from those of the Indonesian-old and other tropical cultivars (Fig. 4b)

213

Field Crops Research 216 (2018) 209–216

A. Saryoko et al.

Table 4 Stomatal morphology and leaf venation length of Experiment 2. Stomatal Morphology†

Group

Lvein

Nstoma (mm−2)

Lguard (μm)

Nepi (mm−2)

SI (%)

Nstoma x Lguard (mm mm−2)

(mm mm−2)

Origin Japan (n = 5) USA (n = 5) Indonesia-old (n = 5) Indonesia-modern (n = 2) Others tropical (n = 3)

279 293 337 327 321

18.4a 18.1ab 17.7ab 17.5ab 17.4b

1209b 1202b 1379a 1329ab 1368a

18.9 19.6 19.7 19.7 19.2

5.15 5.31 5.91 5.95 5.55

5.13b 5.03b 6.06a 6.39a 5.63ab

Region Temperate (n = 10) Tropics (n = 10)

287b 335a

18.2a 17.6b

1219b 1367a

19.1 19.7

5.22b 5.89a

5.17b 5.99a

Average

311.4

17.82

1297

19.4

5.56

5.54

Values followed by the same letters in each column are not significantly different as determined by Tukey’s test at the 5% level. † Values are means of each groups.

the temperate cultivars to be consistently poor, at around one-third to one-fourth of that of the tropical cultivars in both years and that RUE level in 2014 were lower than in 2015 (Table 3), most likely due to the higher level of average SR in 2014 than in 2015 (Table 2), as RUE generally declines with more intense solar radiation and higher fractions of direct radiation (Sinclair et al., 1992). In addition, the CIRR5 and RUE of the temperate cultivars was also half that of the tropical cultivars. In general, the RUE of the temperate cultivars was lower in both 2014 and 2015 than that of the tropical cultivars (Table 3). The RUE of temperate cultivars grown under tropical conditions also tend to be smaller than the RUE of temperate cultivars grown in their region of origin; for instance, the RUE prior to the R5 stage of Enrei grown in Kyoto, Japan (35°01′N) ranged from 0.85–1.06 g MJ−1 (Bajgain et al., 2015), and that of Enrei and Tamahomare—popular commercial cultivars in Japan—grown under various conditions at Shiga, Japan (34°N) ranged from 0.95–1.03 g MJ−1 (Shiraiwa and Hashikawa, 1993). Mean fraction of canopy light interception prior to the R5 (mean FVE-R5) stage was lower in the temperate cultivars than in the tropical cultivars, reflecting differences in growth duration, while the speed of F increase during four WAP did not differ among origin groups (Table 3). This result indicated that both cultivar groups (temperate and tropical), develop canopy at more or less the same rate. In general, there is a linear relationship between the amount of intercepted solar radiation and the net primary production of a given crop (Monteith, 1972, 1977; Shibles and Weber, 1966). However, the shorter growth duration of the temperate cultivars (Table 3) resulted in smaller canopy sizes than that of the tropical cultivars, which displayed longer growth duration. Most notably, RUE of the temperate cultivars was inferior to that of the tropical cultivars. Taken together, the shorter growth duration, smaller canopy size, subsequently poorer CIRR5, and lower energy-utilization efficiency resulted in smaller biomass accumulation among the temperate cultivars.

poorly under the tropical conditions of Indonesia in terms of seed yield and biomass production, even when differences in growth duration were taken into account (Saryoko et al., 2017). For instance, seed yield of the Japanese Enrei cultivar grown in Japan is considerably high ranged from 394 to 405 g m−2 in Takatsuki (34°50′N) and ranged from 403 to 483 in Kyoto (35°01′N) (Tacarindua et al., 2013; Bajgain et al., 2015). However, the seed yield performance of Enrei grown under tropical conditions (∼150 g m−2) (Saryoko et al., 2017) less than half that reported by Tacarindua et al. (2013) and Bajgain et al. (2015). In addition, the seed yields of DS25-1, a cultivars originating in the US with a high-temperature tolerance, were 372 and 255 g m−2 in plants grown in North Carolina under furrow-irrigated and non-irrigated conditions, respectively (USDA-ARS, 2017), whereas the seed yield of DS25-1 grown under tropical conditions was 230 g m−2 (Saryoko et al., 2017), lower than that when grown under favorable conditions, but only slightly lower than when grown under non-irrigated conditions in its region of origin (USDA-ARS, 2017). In present study, the mean daily air temperature (27.8 °C) was higher than 22–24 °C as optimum temperature for highest productivity (Hatfield et al., 2011), near the maximum of the favorable temperature range of 16–28 °C for the whole growing season (McBlain et al., 1987), which was higher than the ranges of 15–22 °C, 20–22 °C, and 15–22 °C as the optimum temperatures for the emergence, flowering and maturity stages, respectively (Liu et al., 2008), and slightly higher than 27 °C, which is an optimum temperature for the seed-filling period (Thomas et al., 2010). The fact that tropical cultivars have better seed yield performance as compared to temperate cultivars under the tropics might suggest that tropical cultivars have greater temperature tolerance than temperate cultivars. The amount of intercepted solar radiation is a key determinant of soybean yield, and differences in RUE can account for variation in dry matter productivity (Board, 2004; Loomis and Amthor, 1999; Sinclair and Horie, 1989; Sinclair and Muchow, 1999). We found the TDWR5 of

Table 5 Correlation analysis of relative transpiration activity and its associated factors of Experiment 2. CTd gs Nstoma Nepi SI Lguard Nstoma x Lguard Lvein

−0.616 −0.453* −0.266ns −0.381ns 0.188ns −0.455* −0.164ns

gs

Nstoma

Nepi

SI

Lguard

Nstoma x Lguard

0.597** 0.712** 0.207ns −0.663** 0.530* 0.694**

0.725** 0.787** −0.410ns 0.952** 0.234ns

−0.627** 0.684** 0.151ns 0.634**

−0.059ns 0.746** −0.229ns

−0.254ns −0.613**

0.250ns

**

** P < 0.01. * P < 0.05. ns not significant.

214

Field Crops Research 216 (2018) 209–216

A. Saryoko et al.

Fig. 4. Performance of 13C isotope discrimination (Δ) (a), and leaf nitrogen content (Ncont) (b) of temperate and tropical cultivar group, (Experiment 2). Upper, middle and lower line in the boxes are Q1, median and Q3, respectively. Boxes indicate with the same letters are not significantly different as determined by Tukey’s test at the 5% level. Bars represent the standard error of two to five cultivars within groups. **p < 0.01; *p < 0.05; ns, not significant.

which in turn is based on the gas exchange rate. Although both Japanese and US cultivars originate from temperate regions, the US cultivars had slightly lower CTd (Fig. 1a–c, Fig. 2), and higher Nstoma and SI values (Table 4), as well as significantly higher gs (p = 0.033; data not shown), than the Japanese cultivars. These findings further support the results of our previous research, in which we determined that US cultivars performed better than Japanese cultivars when grown under tropical conditions (Saryoko et al., 2017). Overall, the evidence suggests that physiological activity levels are highly variable among temperate cultivars raised in tropical environments.

Here, we used CTd as an indicator of relative transpiration activity, and found that the temperate cultivars had significantly higher in CTd levels than did the tropical cultivars in both experiments (Fig. 1a–c). Although CTd levels varied between years and between experiments (Figs. 1 and 2), it was clearly evident that CTd levels were higher in the temperate cultivars than in the tropical cultivars across both years and experiments. This result was consistent with the fact that temperate cultivars also exhibited lower leaf gs than the tropical cultivars, and that CTd was correlated with gs (r = −0.616) (Table 5), an indication that under the tropical conditions of Indonesia, temperate cultivars have lower transpiration activity than tropical cultivars. A negative correlation was detected between RUE and CTd, albeit reaching statistical significance in only three of the ten groups (Fig. 2). These results suggested that the differences in energy utilization and in biomass production between the groups of cultivars was attributable to differences in transpiration activity. RUE and CTd varied between cultivar groups and between cultivars within each group (Fig. 2). Some cultivars sourced from different regions were consistent throughout the year (Fig. 2); for example, some tropical cultivars—in particular Wilis (Indonesian-old), Tanggamus (Indonesian-modern), and EC112828 (Other tropical)—with relatively high levels of RUE and transpiration activity showed superior performance over both 2014 and 2015 (Fig. 2), whereas in contrast, some Japanese cultivars—Enrei and Tachinagaha especially—were consistently inferior in RUE and transpiration activity (Fig. 2), strengthening our conclusion that temperate cultivar performance was generally inferior to that of the tropical cultivars when grown in a tropical environment (Saryoko et al., 2017). Correlations between leaf transpiration/photosynthesis capacity and leaf morphological traits previously been reported for soybean (Tanaka et al., 2008; Tanaka and Shiraiwa, 2009). Here, we found that Nstoma was lower in temperate cultivars than in tropical cultivars, whereas in contrast, Lguard of temperate cultivars were markedly larger than those of cultivars from tropical regions. However, Nstoma × Lguard, which reflects gas exchange capacity, was lower in temperate cultivars than in tropical cultivars, indicating that the low gs in the temperate cultivars can be attributed to leaf morphological traits. As gs is also correlated with Nepi and Lvein, SI did not differ between temperate and tropical cultivars. As such, genotypic variation in terms of relative transpiration activity involved differences in leaf morphological traits, in particular Nstoma, between temperate and tropical soybean cultivars when grown under tropical conditions Variation in gs occurred across groups (Fig. 3), although the Δ appeared to be similar among the groups (Fig. 4a). As Δ is a proxy of intercellular CO2 concentration, an unchanged Δ with greater gs in tropical cultivars than in temperate cultivars suggested that tropical cultivars had higher levels of mesophyll activity, indicating that temperate cultivars are inferior not only in relative transpiration activity but also in mesophyll activity (Fig. 4b). In addition, the lower Ncont among the temperate cultivars provides further evidence of lower mesophyll activity in temperate cultivars, as high Ncont is considered to be indicative of high mesophyll activity (Ohsumi et al., 2007), although this can be addressed only after studying leaf photosynthetic rate,

5. Conclusions Under a tropical environment, soybean cultivars from temperate regions were inferior in biomass production before R5 stage compared to cultivars from the tropical region. A short growth duration resulted in smaller canopy light interception and then lower cumulative radiation intercepted. However, the performance of RUE and relative transpiration activity, in terms of CTd, of temperate cultivars were also inferior. This was associated with leaf morphological traits such as stomatal density and total leaf venation. These results indicate that low biomass production in temperate cultivars can be attributed to the cumulative intercepted radiation in the canopy and also to the low RUE. The low RUE in temperate cultivars was correlated with low gas exchange activity, which may be due to the differences in the leaf morphology. Among temperate cultivars, the US cultivars tended to perform better than the Japanese cultivars in gas exchange activity. This study suggested that different performance of temperate and tropical cultivars may be attributable to different responsiveness to temperature that should be studied under controlled conditions. These results improve our understanding of the genotypic variability of soybean adaptation to the high-temperature environment.

Disclosure statement No potential conflict of interest was reported by the authors.

Funding This study was supported by a grant-in-aid for scientific research (No. 25257410) from the Ministry of Education, Culture, Sports, Science and Technology, Japan.

Acknowledgements We thank Dr. Ir. Muchammad Yusron, M. Phil. of AIAT Banten, IAARD, Ministry of Agriculture, for his generous support with conducting the experiments. We also thank the anonymous reviewer for his/her insightful comments and suggestion on this paper. 215

Field Crops Research 216 (2018) 209–216

A. Saryoko et al.

Appendix A. Supplementary data

Mochizuki, A., Shiraiwa, T., Nakagawa, H., Horie, T., 2005. The effect of temperature during the reproductive period on development of reproductive organs and the occurrence of delayed stem senescence in soybean. Jap J. Crop Sci. 74, 339–343. http:// dx.doi.org/10.1626/jcs.74.339. *. Monteith, J.L., 1972. Solar radiation and productivity in tropical ecosystems. J. Appl. Ecol. 9, 747–766. http://dx.doi.org/10.2307/2401901. Monteith, J.L., 1977. Climate and the efficiency of crop production in Britain. Philos. Trans. R. Soc. B: Biol. Sci. 281, 277–294. http://dx.doi.org/10.1098/rstb.1977.0140. Ohsumi, A., Hamasaki, A., Nakagawa, H., Yoshida, H., Shiraiwa, T., Horie, T., 2007. A model explaining genotypic and ontogenetic variation of leaf photosynthetic rate in rice (Oryza sativa) based on leaf nitrogen content and stomatal conductance. Ann. Bot. 99, 265–273. http://dx.doi.org/10.1093/aob/mcl253. Prasad, P.V.V., Boote, K.J., Allen, L. H. Jr., 2006. Adverse high temperature effects on pollen viability, seed-set, seed yield and harvest index of grain-sorghum [Sorghum bicolor (L.) Moench] are more severe at elevated carbon dioxide due to higher tissue temperatures. Agric. For. Meteorol. 139, 237–251. http://dx.doi.org/10.1016/j. agrformet.2006.07.003. Prasad, P.V.V., Thomas, J.M.G., Narayanan, S., 2017. Global warming effect. Encyclopedia of Applied Plant Sci, 2nd edition. pp. 289–299. Purcell, L.C., 2000. Soybean canopy coverage and light interception measurements using digital imagery. Crop Sci. 40, 834–837. http://dx.doi.org/10.2135/cropsci2000. 403834x. Saryoko, A., Homma, K., Lubis, I., Shiraiwa, T., 2017. Plant development and yield components under a tropical environment in soybean cultivars with temperate and tropical origins. Plant Prod. Sci. http://dx.doi.org/10.1080/1343943X.2017. 1356203. in press. Setiyono, T.D., Weiss, A., Specht, J., Bastidas, A.M., Cassman, K.G., Dobermann, A., 2007. Understanding and modeling the effect of temperature and day length on soybean phenology under high-yield conditions. Field Crop. Res. 100, 257–271. http://dx.doi. org/10.1016/j.fcr.2006.07.011. Setiyono, T.D., Cassman, K.G., Specht, J.E., Dobermann, A., Weiss, A., Yang, H., Conley, S.P., Robinson, A.P., Pedersen, P., De Bruin, J.L., 2010. Simulation of soybean growth and yield in near-optimal growth conditions. Field Crop. Res. 119, 161–174. http:// dx.doi.org/10.1016/j.fcr.2010.07.007. Shibles, R.M., Weber, C.R., 1966. Interception of solar radiation and dry matter production by various soybean planting patterns. Crop Sci. 6, 55–59. http://dx.doi.org/ 10.2135/cropsci1966.0011183X000600010017x. Shiraiwa, T., Hashikawa, U., 1993. Variation analysis of efficiency of intercepted radiation conversion in the accumulation of dry matter by soybean. Jpn. J. Crop Sci. 62, 1–8. http://dx.doi.org/10.1626/jcs.62.1. *. Shiraiwa, T., Kawasaki, Y., Homma, K., 2011. Estimation of crop radiation use efficiency. Jpn. J. Crop Sci. 80, 360–364. http://dx.doi.org/10.1626/jcs.80.360. Sinclair, T.R., Horie, T., 1989. Leaf nitrogen, photosynthesis, and crop radiation use efficiency: a review. Crop Sci. 29, 90–98. http://dx.doi.org/10.2135/cropsci1989. 0011183X002900010023x. Sinclair, T.R., Muchow, R.C., 1999. Radiation use efficiency. Adv. Agric. 65, 215–265. http://dx.doi.org/10.2135/cropsci1989.0011183X002900010023x. Sinclair, T.R., Shiraiwa, T., Hammer, G.L., 1992. Variation in crop radiation-use efficiency with increased disuse radiation. Crop Sci. 32, 1281–1284. http://dx.doi.org/10. 2135/cropsci1992.0011183X003200050043x. Smith, J.R., Mengistu, A., Nelson, R.L., Paris, R.L., 2008. Identification of soybean accessions with high germinability in high-temperature environments. Crop Sci. 48, 2279–2288. http://dx.doi.org/10.2135/cropsci2008.01.0026. Tacarindua, C.R.P., Shiraiwa, T., Homma, K., Kumagai, E., Sameshima, R., 2012. The response of soybean seed growth characteristics to increased temperature under nearfield conditions in a temperature gradient chamber. Field Crop Res. 131, 26–31. http://dx.doi.org/10.1016/j.fcr.2012.02.006. Tacarindua, C.R.P., Shiraiwa, T., Homma, K., Kumagai, E., Sameshima, R., 2013. The effects of increased temperature on crop growth and yield of soybean grown in a temperature gradient chamber. Field Crop Res. 154, 74–81. http://dx.doi.org/10. 1016/j.fcr.2013.07.021. Tanaka, Y., Shiraiwa, T., 2009. Stem growth habit affects leaf morphology and gas exchange traits in soybean. Ann. Bot. 104, 1293–1299. http://dx.doi.org/10.1093/aob/ mcp240. Tanaka, Y., Shiraiwa, T., Nakajima, A., Sato, J., Nakazaki, T., 2008. Leaf gas exchange activity in soybean as related to leaf traits and stem growth habit. Crop Sci. 48, 1925–1932. http://dx.doi.org/10.2135/cropsci2007.12.0707. Thomas, J.M.G., Boote, K.J., Pan, D., Allen Jr., L.H., 2010. Elevated temperature delays onset of the reproductive growth and reduces seed growth rate of soybean. J. Agron. Crop Sci. 1, 19–32. http://dx.doi.org/10.1016/S0167-8809(00)00224-3. United States Department of Agriculture – Agricultural Research Service (USDA-ARS), 2017. Notice of Release of Soybean Germplasm Line DS25-1 with Seed Germination and Seed Quality Tolerance to High Temperature Production Environments. USDAARS, Washington D.C., USA. Wu, T. ting, Li, J. yu, Wu, C. xiang, Sun, S., Mao, T. ting, Jiang, B. jun, Hou, W. sheng, Han, T. fu, 2015. Analysis of the independent- and interactive-photo-thermal effects on soybean flowering. J. Integr. Agric. 14, 622–632. http://dx.doi.org/10.1016/ S2095-3119(14)60856-X.

Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.fcr.2017.11.012. References11*In Japanese with English Abstract. Bajgain, R., Kawasaki, Y., Akamatsu, Y., Tanaka, Y., Kawamura, H., Katsura, K., Shiraiwa, T., 2015. Biomass production and yield of soybean grown under converted paddy fields with excess water during the early growth stage. Field Crop. Res. 180, 221–227. http://dx.doi.org/10.1016/j.fcr.2015.06.010. Bellaloui, N., Smith, J.R., Mengistu, A., Ray, J.D., Gillen, A.M., 2017. Evaluation of exotically-derived soybean breeding lines for seed yield, germination, damage, and composition under dryland production in the Midsouthern USA. Front. Plant Sci. 8, 1–20. http://dx.doi.org/10.3389/fpls.2017.00176. Board, J.E., 2004. Soybean cultivar differences on light interception and leaf area index during Seed Filling. Agron. J. 96, 305–310. http://dx.doi.org/10.2134/ AGRONJ2004.3050. Chebrolu, K.K., Fritschi, F.B., Ye, S., Krishnan, H.B., Smith, J.R., Gillman, J.D., 2016. Impact of heat stress during seed development on soybean seed metabolome. Metabolomics 12, 28. http://dx.doi.org/10.1007/s11306-015-0941-1. Craufurd, P.Q., Wheeler, T.R., 2009. Climate change and the flowering time of annual crops. J. Exp. Bot. 60, 2529–2539. http://dx.doi.org/10.1093/jxb/erp196. Farquhar, G., O’Leary, M., Berry, J., 1982. On the relationship between carbon isotope discrimination and the Intercellular carbon dioxide concentration in leaves. Aust. J. Plant Physiol. 9, 121. http://dx.doi.org/10.1071/PP9820121. Farquhar, G.D., Ehleringer, J.R., Hubick, K.T., 1989. Carbon isotope discrimination and photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 503–537. http://dx. doi.org/10.1146/annurev.pp.40.060189.002443. Fehr, W.R., Caviness, C.E., 1977. Stages of Soybean Development–Special Report 80. Iowa State University, Ames, IA, pp. 1–12. Food and Agriculture Organization, 2017. Food and Agriculture Data [Data Set]. Retrieved February 8, 2017 from. http://www.fao.org/faostat/en/#data/QC/ visualize. Fukuda, Y., Katayama, H., Tanaka, Y., Nakazaki, T., Shiraiwa, T., 2017. A Novel Sample Preparation Method for Carbon Isotope Composition Analysis in the Soybean Leaflet Using a Leaf Punch. In submission manuscript. Gaynor, L.G., Lawn, R.J., James, A.T., 2011. Agronomic studies on irrigated soybean in southern New South Wales. I. Phenological adaptation of genotypes to sowing date. Crop Pasture Sci. 62, 1056–1066. http://dx.doi.org/10.1071/CP11136. Han, T., Wu, C., Tong, Z., Mentreddy, R.S., Tan, K., Gai, J., 2006. Postflowering photoperiod regulates vegetative growth and reproductive development of soybean. Environ. Exp. Bot. 55, 120–129. http://dx.doi.org/10.1016/j.envexpbot.2004.10. 006. Hatfield, J.L., Boote, K.J., Kimball, B.A.B., Ziska, L.H., Izaurralde, R.C., Ort, D., Thomson, A.M., Wolfe, D., 2011. Climate impacts on agriculture: implications for crop production. Agronomy 103, 351–370. http://dx.doi.org/10.2134/agronj2010.0303. Japan Meteorological Agency, Monthly Climate Statistic [Data Set], 2017, Retrieved October 8, 2017 from http://www.data.jma.go.jp/obd/stats/etrn/view/monthly_s3_ en.php?block_no=47759&view=1. Kantolic, A.G., Slafer, G.A., 2001. Photoperiod sensitivity after flowering and seed number determination in indeterminate soybean cultivars. Field Crop. Res. 72, 109–118. http://dx.doi.org/10.1016/S0378-4290(01)00168-X. Kantolic, A.G., Slafer, G.A., 2005. Reproductive development and yield components in indeterminate soybean as affected by post-flowering photoperiod. Field Crop. Res. 93, 212–222. http://dx.doi.org/10.1016/j.fcr.2004.10.001. Kantolic, A.G., Slafer, G.A., 2007. Development and seed number in indeterminate soybean as affected by timing and duration of exposure to long photoperiods after flowering. Ann. Bot. 99, 925–933. http://dx.doi.org/10.1093/aob/mcm033. Kantolic, G., Peralta, G.E., Slafer, G.A., 2013. Seed number responses to extended photoperiod and shading during reproductive stages in indeterminate soybean. Eur. J. Agron. 51, 91–100. http://dx.doi.org/10.1016/j.eja.2013.07.006. Kawasaki, Y., Tanaka, Y., Katsura, K., Purcell, L.C., Shiraiwa, T., 2016. Yield and dry matter productivity of Japanese and US soybean cultivars. Plant Prod. Sci. 19, 257–266. http://dx.doi.org/10.1080/1343943X.2015.1133235. Kumagai, E., Sameshima, R., 2014. Genotypic differences in soybean yield responses to increasing temperature in a cool climate are related to maturity group. Agric. For. Meteorol. 198, 265–272. http://dx.doi.org/10.1016/j.agrformet.2014.08.016. Liu, X., Jin, J., Wang, G., Herbert, S.J., 2008. Soybean yield physiology and development of high-yielding practices in Northeast China. Field Crops Res. 105, 157–171. http:// dx.doi.org/10.1016/j.fcr.2007.09.003. Loomis, R.S., Amthor, J.S., 1999. Yield potential, plant assimilatory capacity, and metabolic efficiencies. Crop Sci. 39, 1584–1596. http://dx.doi.org/10.2135/ cropsci1999.3961584x. McBlain, B.A., Hesketh, J.D., Bernard, R.L., 1987. Genetic effects on reproductive phenology in soybean isolines differing in maturity genes. Can. J. Plant Sci. 67, 105–115. http://dx.doi.org/10.4141/cjps87-012.

216