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Conserved water use improves the yield performance of soybean (Glycine max (L.) Merr.) under drought
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Conserved water use improves the yield performance of soybean (Glycine max (L.) Merr.) under drought Jin He a , Yan-Lei Du a , Tao Wang a , Neil C. Turner b , Ru-Ping Yang c , Yi Jin a , Yue Xi a , Cong Zhang a , Ting Cui a , Xiang-Wen Fang a , Feng-Min Li a,∗ a State Key Laboratory of Grassland Agro-ecosystems, Institute of Arid Agroecology, School of Life Sciences, Lanzhou University, Lanzhou 730000, Gansu Province, China b The Institute of Agriculture, The University of Western Australia, M082, LB 5005, Perth, WA 6001, Australia c Dryland Agriculture Institute, Gansu Academy of Agriculture Sciences, Anning District, Lanzhou 730070, Gansu Province, China
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Article history: Received 30 January 2016 Received in revised form 30 June 2016 Accepted 4 July 2016 Available online xxx Keywords: Drought adaptation Leaf gas exchange Root length density Soybean landraces Terminal water stress Water use efficiency
a b s t r a c t We evaluated the importance of conserved water use in drought adaptation in soybean [Glycine max (L.) Merr.], and identified the traits involved in this mechanism. Eight soybean genotypes, four landraces and four recent cultivars, were collected and yield performance in the field was determined and used in pot experiments to evaluate the yield performance and the water use pattern under three soil moisture treatments imposed from 40 days after sowing: well-watered [WW, soil water content (SWC) maintained between 85%–100% field capacity (FC)]; water stress (WS, water withheld until SWC decreased to 30% FC, rewatered to 100% FC and water withheld again to 30% FC); and terminal water stress (TWS, water withheld until maturity). The recent cultivars all out-yielded the landraces in two different years in the field and under well-watered conditions in the pot experiment. Among the eight soybean genotypes, J19 and ZH – two recent cultivars with lower daily water use before flowering, but higher use after flowering – had the best yield performance in the WS and TWS treatments in the pot experiment and in the field. These two soybean genotypes and J19, another recent cultivar, had higher grain yield, hundred-grain weights and water use efficiency for grain yield (WUEG ) in the WS treatments than the other genotypes, and higher hundred grain weights, higher WUEG , higher pod numbers and the only significant grain yield in the TWS treatment. J19 and ZH had low root length densities (RLD), low leaf areas at flowering, and transpiration decreased at high plant available soil water content under drought. Thus, we conclude that reducing RLD and restricting water loss contributed to conserved water use and improved yield performance and WUEG in water-limited conditions. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Soybean [Glycine max (L.) Merr.] is one of the 10 most-widely grown crops with a total production of over 242 million metric tons in 2012 (FAO stat, http://faostat.fao.org/site/339/default. aspx). Drought stress is a major constraint on the production and yield stability of soybean (Manavalan et al., 2009). Greenhouse and field studies have shown that drought stress leads to a significant reduction (24%–50%) in soybean seed yield (Frederick et al., 2001; Sadeghipour and Abbasi, 2012). Considerable efforts have been
Abbreviations: WW, Well-watered; WS, Cyclic water stress; TWS, Terminal water stress; FC, Field capacity; WUEG , Water use efficiency for grain yield; DAS, Days after sowing; PAWC, Plant available soil water content; SRL, Specific root length; RLD, Root length density; SWC, Soil water content. ∗ Corresponding author. E-mail address: [email protected] (F.-M. Li).
made to enhance drought tolerance in soybean, with the primary goal being to enhance yield under drought conditions. Soybean yields have been improved by traditional breeding and selection, but the physiological basis underlying the yield improvements is largely unknown. A better understanding of the physiological basis for yield gains in water-limited environments will help identify targets for soybean improvement in the future (Koester et al., 2014). Water is the main factor determining the yield performance under drought. Crop yield is dependent on water use during the reproductive stage (Merah, 2001; Kato et al., 2008). It has been reported that final seed yield was negatively affected by water shortage at the flower and pod production stages, and reductions in flower and pod production and flower and pod abortion are key factors affecting final seed yield (Leport et al., 2006; Fang et al., 2010). Under water-limited conditions, water use during the reproductive stage largely depends on water use at the vegetative stage. In pearl millet, lower canopy conductance in terminal drought-tolerant
http://dx.doi.org/10.1016/j.agwat.2016.07.008 0378-3774/© 2016 Elsevier B.V. All rights reserved.
Please cite this article in press as: He, J., et al., Conserved water use improves the yield performance of soybean (Glycine max (L.) Merr.) under drought. Agric. Water Manage. (2016), http://dx.doi.org/10.1016/j.agwat.2016.07.008
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near-isogenic lines saved water under non-stressed conditions, allowing plants to have water available to fill grains (Kholova et al., 2010a,b). This phenomenon was also observed in chickpea (Zaman-Allah et al., 2011). In a modeling study, Sinclair et al. (2010) found that water conservation, through an early decrease in stomatal conductance as the soil began to dry out, had yield benefits under terminal water stress. However, there is no such information for soybean. Water use is determined by water demand and water uptake. Constraining water use can be achieved by having a smaller leaf area and/or less transpiration per unit leaf area. Leaf area can be constrained by reduced tillering (Kim and Luquet, 2010) and branching, reduced leaf number per culm/branch/tiller, and/or reduced individual leaf size (Borrell et al., 2000). Water is also extracted more slowly by a smaller root system (Pantuwan et al., 2002) that may also be associated with a lower leaf area, lower leaf conductance (Vadez et al., 2013) or restricted transpiration at high VPD (Vadez et al., 2014). Faster water use is considered to deplete the water resource by increasing the growth rate of the soybean root system and has a negative effect on soybean yield under water stress (Sinclair et al., 2010). However, previous studies have shown that a greater root density (Carter et al., 1999; Pantalone et al., 1999) and extensive root development contributed to seed yield under terminal drought conditions (Ludlow and Muchow, 1990; Subbarao et al., 1995; Turner et al., 2001; Kashiwagi et al., 2005) because the greater root density improved the extraction of available soil water. Thus, the role of roots in water uptake needs to be further investigated. Obtaining accurate water extraction data in the field is difficult and prone to error. Recently, a method has been developed that uses lysimeters, i.e. long and large PVC tubes filled with natural soil that mimic a real soil profile to determine the water use (Vadez et al., 2008; Ratnakumar et al., 2009). We used long large tubes to determine whether different soybean genotypes have differences water extraction capacities from a soil profile, and whether root length density correlates with water extraction. In northwest China, rainfall is limited during the cropping season, and the grain yield is dependent on the efficient use of rainfall and water stored in the soil. Eight soybean genotypes (four traditional landraces, and four cultivars released after 1998) were used to determine the yield performance in the field during the two growing seasons in two successive years. The same cultivars were used in a lysimeter system to evaluate whether conserved water use will improve the yield of soybean when exposed to transient and terminal water shortage in a rainout shelter. 2. Materials and methods 2.1. Plant materials Eight soybean [Glycine max (L.) Merr.] genotypes, four landraces grown by farmers in Gansu and Shanxi provinces for many generations and four cultivars released between 1999 and 2006 for semiarid and arid regions, were used in this study (Table 1). The lanTable 1 Characteristics of the eight soybean genotypes used in this study. Four genotypes were landraces grown by local farmers in Shanxi or Gansu, and four were recentlyreleased cultivars. Genotypes
Location
Year of release
Huangsedadou (HD) Longxixiaohuangpi (LX) Bailudou (BLD) Xiaoheidou (XHD) Jindou 21 (J21) Jindou 19 (J19) Jidou 12 (J12) Zhonghuang 30 (ZH)
Gansu Gansu Shanxi Shanxi Shanxi Shanxi Hebei Beijing
Landrace Landrace Landrace Landrace 1999 2003 2006 2006
draces were supplied by Chinese Academy of Agricultural Sciences, while Jidou 12 (J12), Jindou 19 (J19) and Zhonghuang 30 (ZH) were supplied by Gansu Academy of Agricultural Sciences, and Jidou 21 (J21) was supplied by Shanxi Academy of Agricultural Sciences. The experiments were conducted at the Yuzhong Experiment Station of Lanzhou University in Yuzhong County, Gansu Province (35◦ 51 N, 104◦ 07 S, altitude 1620 m).
2.2. Field experiment The field experiment was conducted over two successive years, 2011 and 2012. The mean temperature and rainfall during the growing season (April to October) was 14.6 ◦ C and 241 mm in 2011 and 14.4 ◦ C and 343 mm in 2012, respectively. The soil at the site is wind-blown loess and classified as an Entisol (see Wang et al., 2016 for details). Before sowing, 75 kg urea ha−1 and 300 kg calcium superphosphate ha−1 were applied according to local farming practice. The soybeans were grown under rainfed conditions. The individual plot size was 3.0 m wide × 4.0 m long. The soybeans were sown in rows 0.4 m apart giving 18 plants m−2 and with 0.5 m between plots. The experiment was completely randomized with three replications. The plots were kept weed free by hand weeding. At maturity, a 2 m × 2 m subplot was harvested to determine the yield.
2.3. Pot experiment The pot experiment was conducted from 17 April to 19 September 2014. The genotypes were grown in pots in an open rainout shelter that could be closed when rain threatened. The pots were plastic cylinders that were 1.33 m long and 0.16 m in diameter and contained 25.7 kg of sieved loess soil-based substrate (loess soil:vermiculite (v:v) = 3:1). The loess soil was obtained from a field near the site of the field experiment. Transparent polyethylene sleeves (1.4 m long, 0.26 m wide, and 101 m thick) were placed inside the pots prior to filling to allow the contents of the cylinders to be easily removed at harvest. Two seeds were sown in each pot after soaking in water containing 5 g L−1 carbendazim for 600 s to minimize disease. Before sowing, NH4 NO3 and KH2 PO4 fertilizers were added to each pot at a rate of 188 g N g−1 , 27.9 g K g−1 , and 22.1 g P g−1 dry soil. After germination, the seedlings were thinned to one uniform plant per pot. All cylinders were weighed and watered to maintain the soil water content (SWC) between 85%–100% field capacity (FC); 100% FC was determined by watering the soil at 18.00 h [Beijing Standard Time (BST)] until free draining and then allowing the water to drain for 24 h before weighing. Cylinders were weighed on a balance (TCS-100, Jieli Weighting Apparatus Co., Ltd, Yongkang, China) with 2 g accuracy. After thinning, black plastic film was placed on top of the pots to prevent water loss by soil evaporation. In the experiment, phenological development, water use, gas exchange, yield, and yield components of the eight soybean genotypes given three different water treatments were studied. The soybean development stages were as described by Fehr et al. (1971). The three water treatments were imposed from 40 days after sowing (DAS) when the plants were still vegetative with 5–6 trifoliate leaves. The treatments were: (i) well-watered (WW), the soil water content (SWC) was maintained between 85%–100% FC; (ii) cyclic water stress (WS), water withheld until SWC decreased to 30% FC, re-watered to 100% FC, and then allowed to decrease again; and (iii) terminal water stress (TWS) in which water was withheld with no further water added before maturity. In the WS treatment, the cylinders were weighed every 4 days at 06.00 h BST until the SWC decreased to near to 30% FC and then daily until rewatered at 30%
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FC [equivalent to a plant available soil water content (PAWC) of ∼10%] to 100% FC. The following parameters were determined. 2.4. Photosynthesis and predawn leaf water potential Every 4–8 days from 40 to 106 DAS, the fourth leaf from the top was used to determine the predawn leaf water potential, while the third leaf from the top was used to determine the leaf photosynthetic rate, transpiration rate, and stomatal conductance. Each measurement was replicated on the four replicate plants per cultivar per treatment. The predawn leaf water potentials were determined at 04:00–05:00 h BST by the pressure chamber (PMS Instrument Company, 206 Albany, OR, USA) technique using the precautions reported by Turner (1988). The photosynthetic rate, transpiration rate, and stomatal conductance were determined between 08:00 and 10:30 h BST with a model Li-6400 (LiCor Inc., Lincoln, NE, USA) portable gas exchange system. 2.5. Water use determination Plants in the WW treatment were watered every 4 days to maintain the soil between 85%–100% FC until maturity (136–147 DAS), which was defined as occurring when 95% of the pods were brown (Fehr et al., 1971). As soil evaporation was prevented by black plastic film, water use was a measure of whole-plant transpiration. The pots in the water stress treatments (WS and TWS) were weighed every 4–8 days until maturity. Water use was determined by the loss in pot weight in four replicates per cultivar per treatment Water use over the whole life cycle was calculated by adding together the water use between sowing and physiological maturity. Water use from the start of the water treatments (40 DAS) to first flower and first flower to maturity was also calculated. The minimum SWC when no further water loss was observed in the TWS treatment was used to back-calculate the plant available soil water content (PAWC) between 100% FC and this minimum value (∼10% FC) for each measurement of SWC during the drying cycle. 2.6. Root sampling and leaf area at full flowering (R2, 70 DAS) under terminal water stress In the TWS treatment, shoots were cut at ∼10 mm from the soil surface and then divided into leaves and stems. The leaves were scanned by an Epson 10000XL (Epson Inc., Long Beach CA, USA) and leaf area was determined by Image J software (http://imagej. nih.gov/ij/). The polyethylene sleeves for four replicates per genotype were removed from the pots and divided into 0.2 m segments from the surface to 1.2 m depth. The roots in each segment were collected by washing the soil away over a 0.2-mm sieve and the root length obtained by scanning and analyzing the root samples using WinRHIZO Pro (Régent Instruments, Inc, Quebec, Canada). Root length density = root length/soil volume; specific root length = root DW/root length. 2.7. Tagging flowers and pods The start of flowering and podding was recorded for each plant to determine the mean time of flowering and podding for each genotype in the three water treatments. All new flowers and pods were tagged every 2 days with the date of flowering and the date of podding noted on the tags so that flower number, flower abortion, total pod number, pod abortion, filled pod number, and seed number could be determined at physiological maturity. Flower abortion = number of tags with a podding date recorded (tagged pods)/total number of tags (flowers), and pod abortion = filled pod number at physiological maturity/tagged pods.
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2.8. Final yield harvest Four replicates per cultivar per treatment were used to determine the yield and yield components. The plants were harvested when the soybeans were at physiological maturity, the pods and tags removed. The total number of tags was used as a measure of flower number and the number of tags recorded with a podding date as the total pod number. The number of filled pods at physiological maturity was counted, the pods threshed by hand and the grain number counted. Seed size was obtained by weighing 100 oven-dried seeds. The following variable was calculated: water use efficiency (WUEG ) = grain yield/total water use from sowing to maturity. 2.9. Statistical analysis The pot experiment was a randomized complete block design with replicates in blocks. The values for photosynthetic rate, transpiration rate, stomatal conductance and predawn leaf water potential under water stress conditions were expressed relative to the values in the WW treatments. The data are the means of three and four replicates in the field and pot experiments, respectively. The data were analyzed in GenStat 17th Edition (VInternational Ltd., Rothamsted, England) using a generalized linear mixed model (GLMM). The water treatments and genotypes were used as fixed factors and the random factor was block (replicate). 3. Results 3.1. Yield performance in the field experiment and grain yield, water use, and phenology in the pot experiment The grain yield of the eight soybean genotypes varied. The four recent soybean cultivars had significantly higher yields than the four landrace genotypes in the field under rainfed conditions in two successive years (Fig. 1). The grain yields in 2012 were higher than in 2011 and this was likely the consequence of the 40% higher growing-season rainfall in 2012 than 2011. Soybean genotype Jindou 19 (J19) had the highest grain yield and Xiaoheidou (XHD) had the lowest grain yield in the field. In the pot experiment, the time to first flower varied significantly among the eight soybean genotypes (Table 2). As the three water treatments had no significant effect on the days to first flower (Table 2), the data were combined to show that the days to first flower varied in the recent cultivars from 49 DAS in J19 to 68 DAS in J2, but was similar at about 55 DAS in the four landraces (Table 2). The grain yield (GY) and grain size [hundred-grain weight (HGW)] of three of the four recent soybean cultivars were higher than the landraces in the WW treatment (Fig. 2). Among the recent cultivars, J19 had significantly higher grain yield than Zhonghuang 30 (ZH) in the WW treatment that can be explained by the significantly lower HGW of ZH than J19 (Table 2). In the WS treatment, the two soybean cultivars with the earliest flowering time (Table 2), Zhonghuang 30 (ZH) and J19, and the lowest water use (Fig. 2), had higher grain yields and water use efficiencies for grain yield (WUEG ) than the other six soybean genotypes that flowered later and/or had high water use. In the TWS treatment, only two genotypes, ZH and J19, produced a measurable yield (Fig. 2). In the WW treatment, the total water use among the eight soybean genotypes varied significantly (Fig. 2), while water stress (WS and TWS) significantly reduced water use, as expected. The differences in total water use were reflected in the cumulative water use patterns; cultivars J19 and ZH had significantly lower water use than the six other genotypes in the WW treatment (Fig. 3). ZH and J19 had the lowest daily water use before flowering in all three water treatments and
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Fig. 1. the grain yield in the field experiment of the eight soybean cultivars [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)] in 2011 and 2012. Values are means ± one standard error (n = 3). Means with different letters were significantly different at P = 0.05.
Fig. 2. (A) Grain yield (g plant−1 ), (B) filled pod number (plant−1 ), (C) hundred grain weight (g), (D) grain number (plant−1 ), (E) water use efficiency for grain yield (g L−1 ), and (F) water use (L plant−1 ) of eight soybean genotypes [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)] given three water treatments [well-watered (WW); cyclical water stress (WS); and terminal water stress (TWS)] imposed from 40 days after sowing. Values are means ± one standard error of the mean (n = 4). Means with different letters are significantly different at P = 0.05.
the reduced water use before flowering was associated with higher water use after flowering in the WS and TWS treatments (Fig. 4).
3.2. Photosynthesis, stomatal conductance, leaf transpiration, and predawn leaf water potential Water stress (WS and TWS) significantly decreased the predawn leaf water potential (PLWP, % controls): in the four recentlyreleased soybean cultivars, particularly ZH and J19, PLWP in the WS and TWS treatments was unchanged until the PAWC was below
50% (Fig. 5). This threshold PAWC was lower in the recent cultivars, particularly J19, J21 and J12, than the landraces (Fig. 5). In the WS treatment, within 5 days after rewatering, the PLWP recovered to that in the controls before falling again as the soil dried during the second drying cycle. The PLWP fell much more slowly in J12 than in the other genotypes during the second drying cycle. (Fig. 5). The gas exchange parameters also decreased after water was withheld in the WS and TWS treatments (relative to the WW controls) and recovered after rewatering in the WS treatment (Fig. 5). The stomatal conductance (% controls) and leaf transpiration rate (% controls)
Please cite this article in press as: He, J., et al., Conserved water use improves the yield performance of soybean (Glycine max (L.) Merr.) under drought. Agric. Water Manage. (2016), http://dx.doi.org/10.1016/j.agwat.2016.07.008
Flowering time (days)
Flowering period (days)
Podding period (days)
Flower number (plant−1 )
Flower abortion (%)
Tagged pods (plant−1 )
Filled pods (plant−1 )
Pod abortion (%)
Grain yield (g plant−1 )
WW
HD LX BLD XHD J21 J19 J12 ZH Mean
58 61 60 59 68 46 55 52 57
48 45 46 50 44 43 37 36 43
40 36 37 40 32 39 20 31 34
384 591 300 318 469 142 193 134 316
41 50 53 40 59 47 42 46 47
225 293 141 191 195 76 112 73 163
128 147 86 167 133 52 66 52 104
43 50 39 12 32 32 41 28 35
15.3 16.0 13.5 15.5 19.6 19.3 16.6 19.4 16.9
WS
HD LX BLD XHD J21 J19 J12 ZH Mean
56 56 57 54 68 49 64 57 58
40 40 36 42 32 29 15 24 32
30 40 34 39 20 28 16 24 29
184 179 139 179 166 109 114 101 146
38 30 38 25 27 19 37 47 33
114 126 86 133 122 89 72 54 99
78 71 58 80 49 50 48 48 60
31 38 32 40 60 44 33 11 37
7.2 3.3 5.1 6.9 2.3 11.0 8.2 13.5 7.2
TWS
HD LX BLD XHD J21 J19 J12 ZH Mean
56 56 57 54 68 49 64 57 58
19 18 16 20 8 28 16 23 18
8 4 16 15 2 29 12 24 14
111 131 99 61 27 94 72 105 87
88 97 90 93 85 63 76 62 82
14 4 10 5 4 35 17 40 16
0 0 1 0 0 29 12 29 10
100 100 87 100 100 18 28 28 70
0.0 0.0 0.0 0.0 0.0 3.6 0.1 2.4 0.8
GENOTYPE
HD LX BLD XHD J21 J19 J12 ZH Mean W G G×W
56 57 58 56 68 48 61 55 58 n.s ***(2) ***(4)
35 33 34 37 28 33 23 28 31 ***(2) ***(3) ***(5)
26 24 31 31 18 32 16 26 26 **(2) ***(3) ***(5)
226 300 179 186 236 115 107 118 183 ***(35) ***(21) ***(61)
55 58 60 53 61 45 40 48 53 *(5) ***(8) ***(15)
117 143 79 107 106 63 61 61 92 ***(12) ***(20) ***(35)
69 72 48 82 61 42 41 43 57 ***(8) ***(12) ***(21)
58 66 51 49 64 31 32 27 47 *(6) ***(10) ***(17)
7.5 6.5 6.2 7.5 7.3 11.4 9.2 10.8 8.3 ***(0.7) **(1.2) ***(2.1)
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Please cite this article in press as: He, J., et al., Conserved water use improves the yield performance of soybean (Glycine max (L.) Merr.) under drought. Agric. Water Manage. (2016), http://dx.doi.org/10.1016/j.agwat.2016.07.008
Table 2 Flowering time (days), Flowering and podding period (days), flower number (plant-1), flower abortion (%), tagged pods (plant−1 ), filled pods (plant−1 ), pod abortion (%),and grain yield (g plant−1 ) data for the eight soybean genotypes given three water treatments [well-watered (WW, soil water content (SWC) maintained between 85%–100% field capacity (FC)); transient water stress (WS, water withheld until SWC decreased to 30% FC and then rewatered to 100% FC); and terminal water stress (TWS, water withheld to maturity)] imposed from 40 days after sowing. The data were analyzed using a generalized linear mixed model (GLMM), where the water treatments and genotypes were used as fixed factors and the random factor was block (replicate). n.s not significant, *P < 0.05, **P < 0.01, ***P < 0.001. The values in parenthesis are the LSD at P = 0.05.
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Fig. 3. Cumulative water use in eight soybean genotypes [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)] given three water treatments imposed from 40 days after sowing [(a) well watered, (b) cyclical water stress, and (c) terminal water stress]. The vertical arrow in Fig. 3b is the time of rewatering.
of the four landrace genotypes began to decrease at lower values of PAWC than the four recent cultivars in the water stress treatments (Fig. 5). In contrast, the photosynthetic rate (% controls) of the four landrace genotypes decreased at higher PAWC (about 20–40% PAWC) than three of the four recent cultivars (10–15% PAWC) (Fig. 5). The gas exchange parameters recovered more slowly than the PLWP. The leaf transpiration rate never reached that in the WW controls, while the rate of photosynthesis and stomatal conductance recovered faster in the recent cultivars than three of the four landraces (Fig. 5).
Fig. 4. Daily water use from when drought was imposed at 40 DAS to first flower (a) and (b) from first flower to maturity in eight soybean genotypes [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)] under well-watered (WW), cyclical water stress (WS) and terminal water stress (TWS). Values are means ± one standard error of the mean (n = 4). Means with different letters are significantly different at P = 0.05. Note change of scale of y-axis in (a) and (b).
3.4. Leaf area and root morphology At full flowering (R2, 70 DAS) and 30 days after water was withdrawn in the TWS treatment, the leaf area in the recently-released J19 and ZH cultivars was significantly lower than the four landrace genotypes and the remaining two cultivars (Fig. 7). The four recent cultivars had lower root length densities between 0.2 and 1.0 m depth and higher specific root lengths between 0.8 and 1.2 m depth for the roots sampled at the same stage (R2, 70 DAS) (Fig. 8). 4. Discussion 4.1. Yield performance and conserved water use under drought
3.3. Effect of drought on flower and pod number, and flower and pod abortion There was significant variation among the genotypes in the number of flowers, pods, and filled pods produced, and significant variations in the genotype by water stress interaction (Table 2; Fig. 6). In the WW treatment, the four recent soybean cultivars (except J21) produced fewer flowers, fewer tagged pods, and fewer filled pods at maturity than the four landraces, but there were no differences in the length of the flowering period (mean 43.6 days) or podding period (mean 34.4 days) (Table 2). Water stress (WS and TWS) significantly decreased the number of flowers, tagged pods, and filled pods at maturity, shortened the flowering and podding periods, and increased flower and pod abortion (except in WS) relative to the WW treatment (Table 2). ZH and J19 had the longest flowering and podding periods in the TWS treatment (Table 2), and rewatering the pots in the WS treatment induced the recommencement of flower and pod production (Fig. 6).
In this study, we found that drought stress significantly decreased the grain yield and the water use. Among the eight soybean genotypes, in the TWS treatment ZH and J19 with least water use produced some grain, albeit with smaller grain sizes, but the other six soybean genotypes with higher water use produced little or no grain. Moreover, ZH and J19 had the highest yield in the WS treatment (Fig. 2) in which the soybean was rewatered when the SWC was 30% FC and in which flowering commenced again after rewatering. J19 and ZH had the least daily water use before flowering among the eight soybean cultivars under WS and TWS (Fig. 4). Therefore, we suggest that conserved water use before flowering improved yield performance and drought adaptation. This is consistent with previous studies, which showed that conserved water use before flowering is crucial for crops grown under terminal drought (Zaman-Allah et al., 2011; Merah, 2001; Belko et al., 2012; Vadez et al., 2013). A recent study also showed that reducing preflowering water use increased post-anthesis drought adaptation in
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Fig. 5. Relationship between (a) relative predawn leaf water potential, (b) relative rate of photosynthesis, (c) relative stomatal conductance, and (d) relative transpiration rate (% of well-watered control) and plant available soil water content (left column) in eight soybean genotypes [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12) and Zhonghuang (ZH)] under water stress (mean of WS and TWS treatments), and with time after rewatering in the WS treatment (right column).
sorghum (Borrell et al., 2014). Although water use was not monitored, these benefits were also observed in the field experiment. The J19 and ZH cultivars had the highest grain yield under rainfed conditions. Conserved water use was important for the production of some yield, but nevertheless did not restore yields to those in the well-watered soybean. Previous studies have shown that final seed yield was negatively impacted by water shortage during flowering and podding, and that reductions in flower and pod production, and flower and pod abortion are key factors impacting final seed yield in chickpea (Leport et al., 2006; Fang et al., 2010). In this study, the drought stress (WS and TWS) was imposed from 40 DAS and significantly reduced the flower and pod number, increased flower
and pod abortion, and reduced the final yield. In ZH and J19, which showed conserved water use traits, final grain yields, compared to the yields in the WW treatment, were reduced by 19%–44% in the WS treatment, where drought was imposed during flowering and early podding and then relieved by rewatering, and by 82%–86% in the TWS treatment, where drought was imposed during both flowering and podding. However, the reductions in ZH and J19 were less than for the other six genotypes; with the exception of ZH and J19, the other six genotypes under TWS had little or no yield, indicating that the water stress in TWS was quite severe and may have advantaged early-flowering genotypes, J19 and ZH, but disadvantaged late-flowering genotypes. We suggest that this severe water
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Fig. 6. Cumulative flower number (left column) and pod number (right column) with time [days after flowering (left column) and days after podding (right column)] for eight soybean genotypes (Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)) given three water treatments from 40 days after sowing [well watered (WW), cyclical water stress (WS) and terminal water stress (TWS)]. The days between first flowering and first podding are shown in parentheses in the legend for each genotype. Values are means ± one standard error of the mean (n = 4) when larger than the symbol. Note change of scale of y-axis.
Fig. 7. The leaf area of eight soybean genotypes [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)] in the water stress treatment (TWS – water withheld from 40 DAS) at flowering (R2, 70 DAS). Values are means ± one standard error of the mean (n = 4). Means with different letters are significantly different at P = 0.05.
treatment may be useful in mimicking extreme drought events and screening genotypes for high drought tolerance. 4.2. Traits involved in conserved water use Water use by the plant is a function of water loss by the leaves, i.e., the leaf area and leaf transpiration rate, but can also be regu-
lated by the roots, either directly as a result of the root distribution in the soil and/or indirectly by the production of phytohormones, such as ABA, that regulate the stomata in the leaves, and hence water loss by the leaves (Zhang and Davies, 1990). On the demand side, crop water use can be reduced by decreasing transpiration and leaf area. In this study, stomatal conductance and transpiration rate decreased at higher PAWCs in the recent cultivars than in the landraces when water was withdrawn (Fig. 5), maintaining the plant water balance so that the PLWP decreased at lower PAWCs in the recent cultivars than in the landraces and reducing water use. However, the differences in leaf area presumably had the greatest influence on water use with genotypes with high water use also having large leaf areas. ZH and J19, with the lowest water use, had the lowest branch number and leaf area at early podding (Fig. 7). The reduced leaf area was associated with a reduction in branch number and leaf number on the main stem (data not shown). This was consistent with the results of Borrell et al. (2014), who found that leaf area was constrained by reduced tillering and lower leaf number per culm, and that a smaller individual leaf size constrained the leaf area. Earlier flowering may also reduce water use before flowering. Previous studies have shown that alterations to flowering time can minimize the damage caused by terminal drought in wheat (Fleury et al., 2010; Richards et al., 2010). This was consistent with our results showing that the two soybeans ZH and J19 with the earliest flowering time had the highest yield under TWS. Thus, from the demand side, reducing leaf area, and decreasing sto-
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Fig. 8. (a) Root length density, and (b) specific root length of roots at different depths in the soil at flowering (R2, 70 DAS) in the water stress treatment (TWS – water withheld from 40 DAS) in eight soybean genotypes [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)]. Values are means ± one standard error of the mean (n = 4) when larger than the symbol.
matal conductance and transpiration at high PAWCs contributed to conserved water use. On the supply side, improving water accessibility can increase water use at grain filling (van Oosterom et al., 2011), and a number of root-related traits, such as root distribution and root length density, have been proposed as indicators of drought tolerance in soybean (Liu et al., 2005; Wang et al., 2004; Garay and Wilhelm, 1983). In our pot study, we found that the soybean genotypes with smaller water use had lower root length densities (RLD), but higher specific root lengths (SRL) at the same soil depth (Fig. 8), which indicated that root morphology was involved in conserved water use. High SRL means that the root diameter is small and this may constrain water uptake and transport. The important of root morphology in assessing the root hydraulic conductance has been demonstrated by Bramley et al. (2009), but more work needs to be done to evaluate the relationship between the root morphology and root hydraulic conductance. The lower RLD and SRL values may be useful as drought tolerance traits in soybean, but this needs to be evaluated under field conditions where roots are not restricted to a pot. Reductions in the root size and root distribution lead to a fall in the consumption of water and a lower water use. Thus, a population of plants at normal planting density in the field are likely to consume water more slowly and yields would rise under terminal water stress. Reducing the root size and distribution may lower the root hydraulic conductance, which represents the root water uptake and/or transport capacity of a single root or of the whole root system. In this study, the soybean genotypes with lower water use had shorter root length densities. Thus, reducing the RLD may reduce water consumption by lowering water uptake rate, but this needs to be investigated further. 5. Conclusions In this study, we showed that there were variations in water use before flowering among soybean genotypes and that conservative water use was associated with higher yields when subjected to water stress during flowering and podding. The two soybean cultivars, J19 and ZH, with the lowest daily water use and the smallest RLD, had the best yield performance under terminal drought (TWS), when subjected to cycles of water stress (WS), and in the field. The
soybean genotypes with lower water uses before flowering also had lower water uses after flowering when they were adequately watered, but in the TWS treatment, conserved water use before flowering left more water in the soil for use after flowering. This resulted in more flowers, a greater number of pods, and ultimately, a higher yield. Indeed, the only genotypes that produced seeds in the TWS treatment were ZH and J19. Conserved water use also improved the water use efficiency for grain yield (WUEG ) under water-limited conditions; the WUEG in TWS was lower than WS and WW conditions and this can be explained by the very low grain yield in this extreme treatment. Conserved water use by the two genotypes was associated with early flowering, a small leaf area, reductions in stomatal conductance and the transpiration rate at high soil water contents, small root size and low RLD in the waterstressed treatments. Acknowledgements This research was supported by National Natural Science Foundation of China (31300328), the Fundamental Research Funds for the Central Universities (lzujbky-2015-ct02), the ‘111’ Programme (2007B51), and the Program for Innovative Research Teams of Ministry of Education of China (IRT 13R26), the Institute of Agriculture at The University of Western Australia. References Belko, N., Zaman-Allah, M., Cisse, N., Diop, N.N., Zombre, G., Ehlers, J.D., Vadez, V., 2012. Lower soil moisture threshold for transpiration decline under water deficit correlates with lower canopy conductance and higher transpiration efficiency in drought-tolerant cowpea. Funct. Plant Biol. 39, 306. Borrell, A.K., Hammer, G.L., Douglas, A.C., 2000. Does maintaining green leaf area in sorghum improve yield under drought? I. Leaf growth and senescence. Crop Sci. 40, 1026–1037. Borrell, A.K., Mullet, J.E., George-Jaeggli, B., van Oosterom, E.J., Hammer, G.L., Klein, P.E., Jordan, D.R., 2014. Drought adaptation of stay-green sorghum is associated with canopy development, leaf anatomy, root growth, and water uptake. J. Exp. Bot. 65, 6251–6263. Bramley, H., Turner, N.C., Turner, D.W., Tyerman, S.D., 2009. Roles of morphology, anatomy, and aquaporins in determining contrasting hydraulic behavior of roots. Plant Physiol. 150, 348–364. Carter Jr., T.E., De Souza, P.I., Purcell, L.C., 1999. Recent advances in breeding for drought and aluminum resistance in soybean. Proc. World Soybean Conf. VI Chicago, IL, 4–7.
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Conserved water use improves the yield performance of soybean (Glycine max (L.) Merr.) under drought Jin He a , Yan-Lei Du a , Tao Wang a , Neil C. Turner b , Ru-Ping Yang c , Yi Jin a , Yue Xi a , Cong Zhang a , Ting Cui a , Xiang-Wen Fang a , Feng-Min Li a,∗ a State Key Laboratory of Grassland Agro-ecosystems, Institute of Arid Agroecology, School of Life Sciences, Lanzhou University, Lanzhou 730000, Gansu Province, China b The Institute of Agriculture, The University of Western Australia, M082, LB 5005, Perth, WA 6001, Australia c Dryland Agriculture Institute, Gansu Academy of Agriculture Sciences, Anning District, Lanzhou 730070, Gansu Province, China
a r t i c l e
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Article history: Received 30 January 2016 Received in revised form 30 June 2016 Accepted 4 July 2016 Available online xxx Keywords: Drought adaptation Leaf gas exchange Root length density Soybean landraces Terminal water stress Water use efficiency
a b s t r a c t We evaluated the importance of conserved water use in drought adaptation in soybean [Glycine max (L.) Merr.], and identified the traits involved in this mechanism. Eight soybean genotypes, four landraces and four recent cultivars, were collected and yield performance in the field was determined and used in pot experiments to evaluate the yield performance and the water use pattern under three soil moisture treatments imposed from 40 days after sowing: well-watered [WW, soil water content (SWC) maintained between 85%–100% field capacity (FC)]; water stress (WS, water withheld until SWC decreased to 30% FC, rewatered to 100% FC and water withheld again to 30% FC); and terminal water stress (TWS, water withheld until maturity). The recent cultivars all out-yielded the landraces in two different years in the field and under well-watered conditions in the pot experiment. Among the eight soybean genotypes, J19 and ZH – two recent cultivars with lower daily water use before flowering, but higher use after flowering – had the best yield performance in the WS and TWS treatments in the pot experiment and in the field. These two soybean genotypes and J19, another recent cultivar, had higher grain yield, hundred-grain weights and water use efficiency for grain yield (WUEG ) in the WS treatments than the other genotypes, and higher hundred grain weights, higher WUEG , higher pod numbers and the only significant grain yield in the TWS treatment. J19 and ZH had low root length densities (RLD), low leaf areas at flowering, and transpiration decreased at high plant available soil water content under drought. Thus, we conclude that reducing RLD and restricting water loss contributed to conserved water use and improved yield performance and WUEG in water-limited conditions. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Soybean [Glycine max (L.) Merr.] is one of the 10 most-widely grown crops with a total production of over 242 million metric tons in 2012 (FAO stat, http://faostat.fao.org/site/339/default. aspx). Drought stress is a major constraint on the production and yield stability of soybean (Manavalan et al., 2009). Greenhouse and field studies have shown that drought stress leads to a significant reduction (24%–50%) in soybean seed yield (Frederick et al., 2001; Sadeghipour and Abbasi, 2012). Considerable efforts have been
Abbreviations: WW, Well-watered; WS, Cyclic water stress; TWS, Terminal water stress; FC, Field capacity; WUEG , Water use efficiency for grain yield; DAS, Days after sowing; PAWC, Plant available soil water content; SRL, Specific root length; RLD, Root length density; SWC, Soil water content. ∗ Corresponding author. E-mail address: [email protected] (F.-M. Li).
made to enhance drought tolerance in soybean, with the primary goal being to enhance yield under drought conditions. Soybean yields have been improved by traditional breeding and selection, but the physiological basis underlying the yield improvements is largely unknown. A better understanding of the physiological basis for yield gains in water-limited environments will help identify targets for soybean improvement in the future (Koester et al., 2014). Water is the main factor determining the yield performance under drought. Crop yield is dependent on water use during the reproductive stage (Merah, 2001; Kato et al., 2008). It has been reported that final seed yield was negatively affected by water shortage at the flower and pod production stages, and reductions in flower and pod production and flower and pod abortion are key factors affecting final seed yield (Leport et al., 2006; Fang et al., 2010). Under water-limited conditions, water use during the reproductive stage largely depends on water use at the vegetative stage. In pearl millet, lower canopy conductance in terminal drought-tolerant
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near-isogenic lines saved water under non-stressed conditions, allowing plants to have water available to fill grains (Kholova et al., 2010a,b). This phenomenon was also observed in chickpea (Zaman-Allah et al., 2011). In a modeling study, Sinclair et al. (2010) found that water conservation, through an early decrease in stomatal conductance as the soil began to dry out, had yield benefits under terminal water stress. However, there is no such information for soybean. Water use is determined by water demand and water uptake. Constraining water use can be achieved by having a smaller leaf area and/or less transpiration per unit leaf area. Leaf area can be constrained by reduced tillering (Kim and Luquet, 2010) and branching, reduced leaf number per culm/branch/tiller, and/or reduced individual leaf size (Borrell et al., 2000). Water is also extracted more slowly by a smaller root system (Pantuwan et al., 2002) that may also be associated with a lower leaf area, lower leaf conductance (Vadez et al., 2013) or restricted transpiration at high VPD (Vadez et al., 2014). Faster water use is considered to deplete the water resource by increasing the growth rate of the soybean root system and has a negative effect on soybean yield under water stress (Sinclair et al., 2010). However, previous studies have shown that a greater root density (Carter et al., 1999; Pantalone et al., 1999) and extensive root development contributed to seed yield under terminal drought conditions (Ludlow and Muchow, 1990; Subbarao et al., 1995; Turner et al., 2001; Kashiwagi et al., 2005) because the greater root density improved the extraction of available soil water. Thus, the role of roots in water uptake needs to be further investigated. Obtaining accurate water extraction data in the field is difficult and prone to error. Recently, a method has been developed that uses lysimeters, i.e. long and large PVC tubes filled with natural soil that mimic a real soil profile to determine the water use (Vadez et al., 2008; Ratnakumar et al., 2009). We used long large tubes to determine whether different soybean genotypes have differences water extraction capacities from a soil profile, and whether root length density correlates with water extraction. In northwest China, rainfall is limited during the cropping season, and the grain yield is dependent on the efficient use of rainfall and water stored in the soil. Eight soybean genotypes (four traditional landraces, and four cultivars released after 1998) were used to determine the yield performance in the field during the two growing seasons in two successive years. The same cultivars were used in a lysimeter system to evaluate whether conserved water use will improve the yield of soybean when exposed to transient and terminal water shortage in a rainout shelter. 2. Materials and methods 2.1. Plant materials Eight soybean [Glycine max (L.) Merr.] genotypes, four landraces grown by farmers in Gansu and Shanxi provinces for many generations and four cultivars released between 1999 and 2006 for semiarid and arid regions, were used in this study (Table 1). The lanTable 1 Characteristics of the eight soybean genotypes used in this study. Four genotypes were landraces grown by local farmers in Shanxi or Gansu, and four were recentlyreleased cultivars. Genotypes
Location
Year of release
Huangsedadou (HD) Longxixiaohuangpi (LX) Bailudou (BLD) Xiaoheidou (XHD) Jindou 21 (J21) Jindou 19 (J19) Jidou 12 (J12) Zhonghuang 30 (ZH)
Gansu Gansu Shanxi Shanxi Shanxi Shanxi Hebei Beijing
Landrace Landrace Landrace Landrace 1999 2003 2006 2006
draces were supplied by Chinese Academy of Agricultural Sciences, while Jidou 12 (J12), Jindou 19 (J19) and Zhonghuang 30 (ZH) were supplied by Gansu Academy of Agricultural Sciences, and Jidou 21 (J21) was supplied by Shanxi Academy of Agricultural Sciences. The experiments were conducted at the Yuzhong Experiment Station of Lanzhou University in Yuzhong County, Gansu Province (35◦ 51 N, 104◦ 07 S, altitude 1620 m).
2.2. Field experiment The field experiment was conducted over two successive years, 2011 and 2012. The mean temperature and rainfall during the growing season (April to October) was 14.6 ◦ C and 241 mm in 2011 and 14.4 ◦ C and 343 mm in 2012, respectively. The soil at the site is wind-blown loess and classified as an Entisol (see Wang et al., 2016 for details). Before sowing, 75 kg urea ha−1 and 300 kg calcium superphosphate ha−1 were applied according to local farming practice. The soybeans were grown under rainfed conditions. The individual plot size was 3.0 m wide × 4.0 m long. The soybeans were sown in rows 0.4 m apart giving 18 plants m−2 and with 0.5 m between plots. The experiment was completely randomized with three replications. The plots were kept weed free by hand weeding. At maturity, a 2 m × 2 m subplot was harvested to determine the yield.
2.3. Pot experiment The pot experiment was conducted from 17 April to 19 September 2014. The genotypes were grown in pots in an open rainout shelter that could be closed when rain threatened. The pots were plastic cylinders that were 1.33 m long and 0.16 m in diameter and contained 25.7 kg of sieved loess soil-based substrate (loess soil:vermiculite (v:v) = 3:1). The loess soil was obtained from a field near the site of the field experiment. Transparent polyethylene sleeves (1.4 m long, 0.26 m wide, and 101 m thick) were placed inside the pots prior to filling to allow the contents of the cylinders to be easily removed at harvest. Two seeds were sown in each pot after soaking in water containing 5 g L−1 carbendazim for 600 s to minimize disease. Before sowing, NH4 NO3 and KH2 PO4 fertilizers were added to each pot at a rate of 188 g N g−1 , 27.9 g K g−1 , and 22.1 g P g−1 dry soil. After germination, the seedlings were thinned to one uniform plant per pot. All cylinders were weighed and watered to maintain the soil water content (SWC) between 85%–100% field capacity (FC); 100% FC was determined by watering the soil at 18.00 h [Beijing Standard Time (BST)] until free draining and then allowing the water to drain for 24 h before weighing. Cylinders were weighed on a balance (TCS-100, Jieli Weighting Apparatus Co., Ltd, Yongkang, China) with 2 g accuracy. After thinning, black plastic film was placed on top of the pots to prevent water loss by soil evaporation. In the experiment, phenological development, water use, gas exchange, yield, and yield components of the eight soybean genotypes given three different water treatments were studied. The soybean development stages were as described by Fehr et al. (1971). The three water treatments were imposed from 40 days after sowing (DAS) when the plants were still vegetative with 5–6 trifoliate leaves. The treatments were: (i) well-watered (WW), the soil water content (SWC) was maintained between 85%–100% FC; (ii) cyclic water stress (WS), water withheld until SWC decreased to 30% FC, re-watered to 100% FC, and then allowed to decrease again; and (iii) terminal water stress (TWS) in which water was withheld with no further water added before maturity. In the WS treatment, the cylinders were weighed every 4 days at 06.00 h BST until the SWC decreased to near to 30% FC and then daily until rewatered at 30%
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FC [equivalent to a plant available soil water content (PAWC) of ∼10%] to 100% FC. The following parameters were determined. 2.4. Photosynthesis and predawn leaf water potential Every 4–8 days from 40 to 106 DAS, the fourth leaf from the top was used to determine the predawn leaf water potential, while the third leaf from the top was used to determine the leaf photosynthetic rate, transpiration rate, and stomatal conductance. Each measurement was replicated on the four replicate plants per cultivar per treatment. The predawn leaf water potentials were determined at 04:00–05:00 h BST by the pressure chamber (PMS Instrument Company, 206 Albany, OR, USA) technique using the precautions reported by Turner (1988). The photosynthetic rate, transpiration rate, and stomatal conductance were determined between 08:00 and 10:30 h BST with a model Li-6400 (LiCor Inc., Lincoln, NE, USA) portable gas exchange system. 2.5. Water use determination Plants in the WW treatment were watered every 4 days to maintain the soil between 85%–100% FC until maturity (136–147 DAS), which was defined as occurring when 95% of the pods were brown (Fehr et al., 1971). As soil evaporation was prevented by black plastic film, water use was a measure of whole-plant transpiration. The pots in the water stress treatments (WS and TWS) were weighed every 4–8 days until maturity. Water use was determined by the loss in pot weight in four replicates per cultivar per treatment Water use over the whole life cycle was calculated by adding together the water use between sowing and physiological maturity. Water use from the start of the water treatments (40 DAS) to first flower and first flower to maturity was also calculated. The minimum SWC when no further water loss was observed in the TWS treatment was used to back-calculate the plant available soil water content (PAWC) between 100% FC and this minimum value (∼10% FC) for each measurement of SWC during the drying cycle. 2.6. Root sampling and leaf area at full flowering (R2, 70 DAS) under terminal water stress In the TWS treatment, shoots were cut at ∼10 mm from the soil surface and then divided into leaves and stems. The leaves were scanned by an Epson 10000XL (Epson Inc., Long Beach CA, USA) and leaf area was determined by Image J software (http://imagej. nih.gov/ij/). The polyethylene sleeves for four replicates per genotype were removed from the pots and divided into 0.2 m segments from the surface to 1.2 m depth. The roots in each segment were collected by washing the soil away over a 0.2-mm sieve and the root length obtained by scanning and analyzing the root samples using WinRHIZO Pro (Régent Instruments, Inc, Quebec, Canada). Root length density = root length/soil volume; specific root length = root DW/root length. 2.7. Tagging flowers and pods The start of flowering and podding was recorded for each plant to determine the mean time of flowering and podding for each genotype in the three water treatments. All new flowers and pods were tagged every 2 days with the date of flowering and the date of podding noted on the tags so that flower number, flower abortion, total pod number, pod abortion, filled pod number, and seed number could be determined at physiological maturity. Flower abortion = number of tags with a podding date recorded (tagged pods)/total number of tags (flowers), and pod abortion = filled pod number at physiological maturity/tagged pods.
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2.8. Final yield harvest Four replicates per cultivar per treatment were used to determine the yield and yield components. The plants were harvested when the soybeans were at physiological maturity, the pods and tags removed. The total number of tags was used as a measure of flower number and the number of tags recorded with a podding date as the total pod number. The number of filled pods at physiological maturity was counted, the pods threshed by hand and the grain number counted. Seed size was obtained by weighing 100 oven-dried seeds. The following variable was calculated: water use efficiency (WUEG ) = grain yield/total water use from sowing to maturity. 2.9. Statistical analysis The pot experiment was a randomized complete block design with replicates in blocks. The values for photosynthetic rate, transpiration rate, stomatal conductance and predawn leaf water potential under water stress conditions were expressed relative to the values in the WW treatments. The data are the means of three and four replicates in the field and pot experiments, respectively. The data were analyzed in GenStat 17th Edition (VInternational Ltd., Rothamsted, England) using a generalized linear mixed model (GLMM). The water treatments and genotypes were used as fixed factors and the random factor was block (replicate). 3. Results 3.1. Yield performance in the field experiment and grain yield, water use, and phenology in the pot experiment The grain yield of the eight soybean genotypes varied. The four recent soybean cultivars had significantly higher yields than the four landrace genotypes in the field under rainfed conditions in two successive years (Fig. 1). The grain yields in 2012 were higher than in 2011 and this was likely the consequence of the 40% higher growing-season rainfall in 2012 than 2011. Soybean genotype Jindou 19 (J19) had the highest grain yield and Xiaoheidou (XHD) had the lowest grain yield in the field. In the pot experiment, the time to first flower varied significantly among the eight soybean genotypes (Table 2). As the three water treatments had no significant effect on the days to first flower (Table 2), the data were combined to show that the days to first flower varied in the recent cultivars from 49 DAS in J19 to 68 DAS in J2, but was similar at about 55 DAS in the four landraces (Table 2). The grain yield (GY) and grain size [hundred-grain weight (HGW)] of three of the four recent soybean cultivars were higher than the landraces in the WW treatment (Fig. 2). Among the recent cultivars, J19 had significantly higher grain yield than Zhonghuang 30 (ZH) in the WW treatment that can be explained by the significantly lower HGW of ZH than J19 (Table 2). In the WS treatment, the two soybean cultivars with the earliest flowering time (Table 2), Zhonghuang 30 (ZH) and J19, and the lowest water use (Fig. 2), had higher grain yields and water use efficiencies for grain yield (WUEG ) than the other six soybean genotypes that flowered later and/or had high water use. In the TWS treatment, only two genotypes, ZH and J19, produced a measurable yield (Fig. 2). In the WW treatment, the total water use among the eight soybean genotypes varied significantly (Fig. 2), while water stress (WS and TWS) significantly reduced water use, as expected. The differences in total water use were reflected in the cumulative water use patterns; cultivars J19 and ZH had significantly lower water use than the six other genotypes in the WW treatment (Fig. 3). ZH and J19 had the lowest daily water use before flowering in all three water treatments and
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Fig. 1. the grain yield in the field experiment of the eight soybean cultivars [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)] in 2011 and 2012. Values are means ± one standard error (n = 3). Means with different letters were significantly different at P = 0.05.
Fig. 2. (A) Grain yield (g plant−1 ), (B) filled pod number (plant−1 ), (C) hundred grain weight (g), (D) grain number (plant−1 ), (E) water use efficiency for grain yield (g L−1 ), and (F) water use (L plant−1 ) of eight soybean genotypes [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)] given three water treatments [well-watered (WW); cyclical water stress (WS); and terminal water stress (TWS)] imposed from 40 days after sowing. Values are means ± one standard error of the mean (n = 4). Means with different letters are significantly different at P = 0.05.
the reduced water use before flowering was associated with higher water use after flowering in the WS and TWS treatments (Fig. 4).
3.2. Photosynthesis, stomatal conductance, leaf transpiration, and predawn leaf water potential Water stress (WS and TWS) significantly decreased the predawn leaf water potential (PLWP, % controls): in the four recentlyreleased soybean cultivars, particularly ZH and J19, PLWP in the WS and TWS treatments was unchanged until the PAWC was below
50% (Fig. 5). This threshold PAWC was lower in the recent cultivars, particularly J19, J21 and J12, than the landraces (Fig. 5). In the WS treatment, within 5 days after rewatering, the PLWP recovered to that in the controls before falling again as the soil dried during the second drying cycle. The PLWP fell much more slowly in J12 than in the other genotypes during the second drying cycle. (Fig. 5). The gas exchange parameters also decreased after water was withheld in the WS and TWS treatments (relative to the WW controls) and recovered after rewatering in the WS treatment (Fig. 5). The stomatal conductance (% controls) and leaf transpiration rate (% controls)
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Flowering time (days)
Flowering period (days)
Podding period (days)
Flower number (plant−1 )
Flower abortion (%)
Tagged pods (plant−1 )
Filled pods (plant−1 )
Pod abortion (%)
Grain yield (g plant−1 )
WW
HD LX BLD XHD J21 J19 J12 ZH Mean
58 61 60 59 68 46 55 52 57
48 45 46 50 44 43 37 36 43
40 36 37 40 32 39 20 31 34
384 591 300 318 469 142 193 134 316
41 50 53 40 59 47 42 46 47
225 293 141 191 195 76 112 73 163
128 147 86 167 133 52 66 52 104
43 50 39 12 32 32 41 28 35
15.3 16.0 13.5 15.5 19.6 19.3 16.6 19.4 16.9
WS
HD LX BLD XHD J21 J19 J12 ZH Mean
56 56 57 54 68 49 64 57 58
40 40 36 42 32 29 15 24 32
30 40 34 39 20 28 16 24 29
184 179 139 179 166 109 114 101 146
38 30 38 25 27 19 37 47 33
114 126 86 133 122 89 72 54 99
78 71 58 80 49 50 48 48 60
31 38 32 40 60 44 33 11 37
7.2 3.3 5.1 6.9 2.3 11.0 8.2 13.5 7.2
TWS
HD LX BLD XHD J21 J19 J12 ZH Mean
56 56 57 54 68 49 64 57 58
19 18 16 20 8 28 16 23 18
8 4 16 15 2 29 12 24 14
111 131 99 61 27 94 72 105 87
88 97 90 93 85 63 76 62 82
14 4 10 5 4 35 17 40 16
0 0 1 0 0 29 12 29 10
100 100 87 100 100 18 28 28 70
0.0 0.0 0.0 0.0 0.0 3.6 0.1 2.4 0.8
GENOTYPE
HD LX BLD XHD J21 J19 J12 ZH Mean W G G×W
56 57 58 56 68 48 61 55 58 n.s ***(2) ***(4)
35 33 34 37 28 33 23 28 31 ***(2) ***(3) ***(5)
26 24 31 31 18 32 16 26 26 **(2) ***(3) ***(5)
226 300 179 186 236 115 107 118 183 ***(35) ***(21) ***(61)
55 58 60 53 61 45 40 48 53 *(5) ***(8) ***(15)
117 143 79 107 106 63 61 61 92 ***(12) ***(20) ***(35)
69 72 48 82 61 42 41 43 57 ***(8) ***(12) ***(21)
58 66 51 49 64 31 32 27 47 *(6) ***(10) ***(17)
7.5 6.5 6.2 7.5 7.3 11.4 9.2 10.8 8.3 ***(0.7) **(1.2) ***(2.1)
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Table 2 Flowering time (days), Flowering and podding period (days), flower number (plant-1), flower abortion (%), tagged pods (plant−1 ), filled pods (plant−1 ), pod abortion (%),and grain yield (g plant−1 ) data for the eight soybean genotypes given three water treatments [well-watered (WW, soil water content (SWC) maintained between 85%–100% field capacity (FC)); transient water stress (WS, water withheld until SWC decreased to 30% FC and then rewatered to 100% FC); and terminal water stress (TWS, water withheld to maturity)] imposed from 40 days after sowing. The data were analyzed using a generalized linear mixed model (GLMM), where the water treatments and genotypes were used as fixed factors and the random factor was block (replicate). n.s not significant, *P < 0.05, **P < 0.01, ***P < 0.001. The values in parenthesis are the LSD at P = 0.05.
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Fig. 3. Cumulative water use in eight soybean genotypes [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)] given three water treatments imposed from 40 days after sowing [(a) well watered, (b) cyclical water stress, and (c) terminal water stress]. The vertical arrow in Fig. 3b is the time of rewatering.
of the four landrace genotypes began to decrease at lower values of PAWC than the four recent cultivars in the water stress treatments (Fig. 5). In contrast, the photosynthetic rate (% controls) of the four landrace genotypes decreased at higher PAWC (about 20–40% PAWC) than three of the four recent cultivars (10–15% PAWC) (Fig. 5). The gas exchange parameters recovered more slowly than the PLWP. The leaf transpiration rate never reached that in the WW controls, while the rate of photosynthesis and stomatal conductance recovered faster in the recent cultivars than three of the four landraces (Fig. 5).
Fig. 4. Daily water use from when drought was imposed at 40 DAS to first flower (a) and (b) from first flower to maturity in eight soybean genotypes [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)] under well-watered (WW), cyclical water stress (WS) and terminal water stress (TWS). Values are means ± one standard error of the mean (n = 4). Means with different letters are significantly different at P = 0.05. Note change of scale of y-axis in (a) and (b).
3.4. Leaf area and root morphology At full flowering (R2, 70 DAS) and 30 days after water was withdrawn in the TWS treatment, the leaf area in the recently-released J19 and ZH cultivars was significantly lower than the four landrace genotypes and the remaining two cultivars (Fig. 7). The four recent cultivars had lower root length densities between 0.2 and 1.0 m depth and higher specific root lengths between 0.8 and 1.2 m depth for the roots sampled at the same stage (R2, 70 DAS) (Fig. 8). 4. Discussion 4.1. Yield performance and conserved water use under drought
3.3. Effect of drought on flower and pod number, and flower and pod abortion There was significant variation among the genotypes in the number of flowers, pods, and filled pods produced, and significant variations in the genotype by water stress interaction (Table 2; Fig. 6). In the WW treatment, the four recent soybean cultivars (except J21) produced fewer flowers, fewer tagged pods, and fewer filled pods at maturity than the four landraces, but there were no differences in the length of the flowering period (mean 43.6 days) or podding period (mean 34.4 days) (Table 2). Water stress (WS and TWS) significantly decreased the number of flowers, tagged pods, and filled pods at maturity, shortened the flowering and podding periods, and increased flower and pod abortion (except in WS) relative to the WW treatment (Table 2). ZH and J19 had the longest flowering and podding periods in the TWS treatment (Table 2), and rewatering the pots in the WS treatment induced the recommencement of flower and pod production (Fig. 6).
In this study, we found that drought stress significantly decreased the grain yield and the water use. Among the eight soybean genotypes, in the TWS treatment ZH and J19 with least water use produced some grain, albeit with smaller grain sizes, but the other six soybean genotypes with higher water use produced little or no grain. Moreover, ZH and J19 had the highest yield in the WS treatment (Fig. 2) in which the soybean was rewatered when the SWC was 30% FC and in which flowering commenced again after rewatering. J19 and ZH had the least daily water use before flowering among the eight soybean cultivars under WS and TWS (Fig. 4). Therefore, we suggest that conserved water use before flowering improved yield performance and drought adaptation. This is consistent with previous studies, which showed that conserved water use before flowering is crucial for crops grown under terminal drought (Zaman-Allah et al., 2011; Merah, 2001; Belko et al., 2012; Vadez et al., 2013). A recent study also showed that reducing preflowering water use increased post-anthesis drought adaptation in
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Fig. 5. Relationship between (a) relative predawn leaf water potential, (b) relative rate of photosynthesis, (c) relative stomatal conductance, and (d) relative transpiration rate (% of well-watered control) and plant available soil water content (left column) in eight soybean genotypes [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12) and Zhonghuang (ZH)] under water stress (mean of WS and TWS treatments), and with time after rewatering in the WS treatment (right column).
sorghum (Borrell et al., 2014). Although water use was not monitored, these benefits were also observed in the field experiment. The J19 and ZH cultivars had the highest grain yield under rainfed conditions. Conserved water use was important for the production of some yield, but nevertheless did not restore yields to those in the well-watered soybean. Previous studies have shown that final seed yield was negatively impacted by water shortage during flowering and podding, and that reductions in flower and pod production, and flower and pod abortion are key factors impacting final seed yield in chickpea (Leport et al., 2006; Fang et al., 2010). In this study, the drought stress (WS and TWS) was imposed from 40 DAS and significantly reduced the flower and pod number, increased flower
and pod abortion, and reduced the final yield. In ZH and J19, which showed conserved water use traits, final grain yields, compared to the yields in the WW treatment, were reduced by 19%–44% in the WS treatment, where drought was imposed during flowering and early podding and then relieved by rewatering, and by 82%–86% in the TWS treatment, where drought was imposed during both flowering and podding. However, the reductions in ZH and J19 were less than for the other six genotypes; with the exception of ZH and J19, the other six genotypes under TWS had little or no yield, indicating that the water stress in TWS was quite severe and may have advantaged early-flowering genotypes, J19 and ZH, but disadvantaged late-flowering genotypes. We suggest that this severe water
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Fig. 6. Cumulative flower number (left column) and pod number (right column) with time [days after flowering (left column) and days after podding (right column)] for eight soybean genotypes (Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)) given three water treatments from 40 days after sowing [well watered (WW), cyclical water stress (WS) and terminal water stress (TWS)]. The days between first flowering and first podding are shown in parentheses in the legend for each genotype. Values are means ± one standard error of the mean (n = 4) when larger than the symbol. Note change of scale of y-axis.
Fig. 7. The leaf area of eight soybean genotypes [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)] in the water stress treatment (TWS – water withheld from 40 DAS) at flowering (R2, 70 DAS). Values are means ± one standard error of the mean (n = 4). Means with different letters are significantly different at P = 0.05.
treatment may be useful in mimicking extreme drought events and screening genotypes for high drought tolerance. 4.2. Traits involved in conserved water use Water use by the plant is a function of water loss by the leaves, i.e., the leaf area and leaf transpiration rate, but can also be regu-
lated by the roots, either directly as a result of the root distribution in the soil and/or indirectly by the production of phytohormones, such as ABA, that regulate the stomata in the leaves, and hence water loss by the leaves (Zhang and Davies, 1990). On the demand side, crop water use can be reduced by decreasing transpiration and leaf area. In this study, stomatal conductance and transpiration rate decreased at higher PAWCs in the recent cultivars than in the landraces when water was withdrawn (Fig. 5), maintaining the plant water balance so that the PLWP decreased at lower PAWCs in the recent cultivars than in the landraces and reducing water use. However, the differences in leaf area presumably had the greatest influence on water use with genotypes with high water use also having large leaf areas. ZH and J19, with the lowest water use, had the lowest branch number and leaf area at early podding (Fig. 7). The reduced leaf area was associated with a reduction in branch number and leaf number on the main stem (data not shown). This was consistent with the results of Borrell et al. (2014), who found that leaf area was constrained by reduced tillering and lower leaf number per culm, and that a smaller individual leaf size constrained the leaf area. Earlier flowering may also reduce water use before flowering. Previous studies have shown that alterations to flowering time can minimize the damage caused by terminal drought in wheat (Fleury et al., 2010; Richards et al., 2010). This was consistent with our results showing that the two soybeans ZH and J19 with the earliest flowering time had the highest yield under TWS. Thus, from the demand side, reducing leaf area, and decreasing sto-
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Fig. 8. (a) Root length density, and (b) specific root length of roots at different depths in the soil at flowering (R2, 70 DAS) in the water stress treatment (TWS – water withheld from 40 DAS) in eight soybean genotypes [Huangsedadou (HD), Longxixiaohuangpi (LX), Bailudou (BLD), Xiaoheidou (XHD), Jindou 21 (J21), Jindou 19 (J19), Jidou 12 (J12), and Zhonghuang (ZH)]. Values are means ± one standard error of the mean (n = 4) when larger than the symbol.
matal conductance and transpiration at high PAWCs contributed to conserved water use. On the supply side, improving water accessibility can increase water use at grain filling (van Oosterom et al., 2011), and a number of root-related traits, such as root distribution and root length density, have been proposed as indicators of drought tolerance in soybean (Liu et al., 2005; Wang et al., 2004; Garay and Wilhelm, 1983). In our pot study, we found that the soybean genotypes with smaller water use had lower root length densities (RLD), but higher specific root lengths (SRL) at the same soil depth (Fig. 8), which indicated that root morphology was involved in conserved water use. High SRL means that the root diameter is small and this may constrain water uptake and transport. The important of root morphology in assessing the root hydraulic conductance has been demonstrated by Bramley et al. (2009), but more work needs to be done to evaluate the relationship between the root morphology and root hydraulic conductance. The lower RLD and SRL values may be useful as drought tolerance traits in soybean, but this needs to be evaluated under field conditions where roots are not restricted to a pot. Reductions in the root size and root distribution lead to a fall in the consumption of water and a lower water use. Thus, a population of plants at normal planting density in the field are likely to consume water more slowly and yields would rise under terminal water stress. Reducing the root size and distribution may lower the root hydraulic conductance, which represents the root water uptake and/or transport capacity of a single root or of the whole root system. In this study, the soybean genotypes with lower water use had shorter root length densities. Thus, reducing the RLD may reduce water consumption by lowering water uptake rate, but this needs to be investigated further. 5. Conclusions In this study, we showed that there were variations in water use before flowering among soybean genotypes and that conservative water use was associated with higher yields when subjected to water stress during flowering and podding. The two soybean cultivars, J19 and ZH, with the lowest daily water use and the smallest RLD, had the best yield performance under terminal drought (TWS), when subjected to cycles of water stress (WS), and in the field. The
soybean genotypes with lower water uses before flowering also had lower water uses after flowering when they were adequately watered, but in the TWS treatment, conserved water use before flowering left more water in the soil for use after flowering. This resulted in more flowers, a greater number of pods, and ultimately, a higher yield. Indeed, the only genotypes that produced seeds in the TWS treatment were ZH and J19. Conserved water use also improved the water use efficiency for grain yield (WUEG ) under water-limited conditions; the WUEG in TWS was lower than WS and WW conditions and this can be explained by the very low grain yield in this extreme treatment. Conserved water use by the two genotypes was associated with early flowering, a small leaf area, reductions in stomatal conductance and the transpiration rate at high soil water contents, small root size and low RLD in the waterstressed treatments. Acknowledgements This research was supported by National Natural Science Foundation of China (31300328), the Fundamental Research Funds for the Central Universities (lzujbky-2015-ct02), the ‘111’ Programme (2007B51), and the Program for Innovative Research Teams of Ministry of Education of China (IRT 13R26), the Institute of Agriculture at The University of Western Australia. References Belko, N., Zaman-Allah, M., Cisse, N., Diop, N.N., Zombre, G., Ehlers, J.D., Vadez, V., 2012. Lower soil moisture threshold for transpiration decline under water deficit correlates with lower canopy conductance and higher transpiration efficiency in drought-tolerant cowpea. Funct. Plant Biol. 39, 306. Borrell, A.K., Hammer, G.L., Douglas, A.C., 2000. Does maintaining green leaf area in sorghum improve yield under drought? I. Leaf growth and senescence. Crop Sci. 40, 1026–1037. Borrell, A.K., Mullet, J.E., George-Jaeggli, B., van Oosterom, E.J., Hammer, G.L., Klein, P.E., Jordan, D.R., 2014. Drought adaptation of stay-green sorghum is associated with canopy development, leaf anatomy, root growth, and water uptake. J. Exp. Bot. 65, 6251–6263. Bramley, H., Turner, N.C., Turner, D.W., Tyerman, S.D., 2009. Roles of morphology, anatomy, and aquaporins in determining contrasting hydraulic behavior of roots. Plant Physiol. 150, 348–364. Carter Jr., T.E., De Souza, P.I., Purcell, L.C., 1999. Recent advances in breeding for drought and aluminum resistance in soybean. Proc. World Soybean Conf. VI Chicago, IL, 4–7.
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Please cite this article in press as: He, J., et al., Conserved water use improves the yield performance of soybean (Glycine max (L.) Merr.) under drought. Agric. Water Manage. (2016), http://dx.doi.org/10.1016/j.agwat.2016.07.008