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Maintained root length density contributes to the waterlogging tolerance in common wheat (Triticum aestivum L.)
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Maintained root length density contributes to the waterlogging tolerance in common wheat (Triticum aestivum L.) Tomohito Hayashi a , Tomofumi Yoshida b , Kiyoshi Fujii b,c , Shiro Mitsuya a , Takako Tsuji b , Yurie Okada a , Eriko Hayashi a , Akira Yamauchi a,∗ a
Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan Aichi Prefecture Agricultural Research Center, 1-1, Aza-Sagamine, Oaza-Yazako, Nagakute-cho, Aichi-gun 480-1193, Japan c Agricultural Production Division, Aichi Prefectural Government, 3-1-2, Sannomaru, Naka-ku, Nagoya 460-8501, Japan b
a r t i c l e
i n f o
Article history: Received 31 October 2012 Received in revised form 25 March 2013 Accepted 30 March 2013 Keywords: Common wheat Triticum aestivum L. Grain yield Root length density Waterlogging
a b s t r a c t Waterlogging stress substantially reduces the growth and yield of common wheat (Triticum aestivum L.). Limited root development due to decreased availability of oxygen in roots is the major growth-limiting factor for plants under waterlogged conditions. In this study, we have determined whether a maintained root length density can be one of the important traits for waterlogging tolerance to maintain the shoot growth and grain yield, using waterlogging-tolerant and -susceptible wheat cultivars. This study was carried out over five consecutive cropping seasons (from 2006 to 2010), and the wheat plants were exposed to waterlogging from jointing stage to maturity. The waterlogging-tolerant cultivars Nishikazekomugi and Iwainodaichi showed higher relative grain yield and whole grain ratio under waterlogged conditions than the susceptible UNICULM. The waterlogging-tolerant cultivars maintained higher leaf water potential, stomatal conductance and photosynthetic rate under waterlogged conditions than the susceptible one, which was consistent with the higher relative root length density in the tolerant cultivars. These results indicate that maintained root length density is related to maintaining water uptake and the resultant photosynthesis and yield production in common wheat grown under waterlogged conditions. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Common wheat (Triticum aestivum) is an important staple crop plant together with rice and maize, and its production reached 610 million tons in 2007 (FAO, 2009). Wheat plants are mainly grown where annual precipitation is around 600–700 mm. Waterlogging is one of the important constraints that reduce the productivity of wheat in Japan, since the annual precipitation is greater than 1000 mm. In addition, wheat is generally cultivated in drained paddy fields that have been converted from paddy field to mitigate the problem of rice overproduction. Large-scale waterlogging in wheat also occurs in irrigated rice–wheat rotation systems in south and east Asia where wheat is cultivated in the fields that have top soil compaction for rice cultivation in flooding conditions (Samad et al., 2001). In the US, more than 10 million ha is affected by excess
∗ Corresponding author. Tel.: +81 52 789 4022; fax: +81 52 789 4022. E-mail addresses: [email protected] (T. Hayashi), tomofumi [email protected] (T. Yoshida), kiyoshi [email protected] (K. Fujii), [email protected] (S. Mitsuya), takako [email protected] (T. Tsuji), [email protected] (A. Yamauchi).
water conditions, which is equivalent to 12% of the total cultivated land (Boyer, 1982). Therefore, the improvement of waterlogging tolerance is an important target to increase and stabilize wheat production. When plants are exposed to waterlogged conditions, the availability of oxygen in the rhizosphere becomes limited (Ponnamperuma, 1972). Because oxygen is necessary for the respiration in roots, oxygen deficiency caused by waterlogging affects root growth and consequently reduces the shoot growth and yield (Malik et al., 2002; Colmer and Voesenek, 2009). The impact of waterlogging on the plant growth varies with different developmental stages. Waterlogging during the vegetative stage reduces grain yield due to a decrease in tiller number (Cannell and Belford, 1980; Belford, 1981; Cannell et al., 1984; Sharma and Swarup, 1988; Musgrave, 1994; Musgrave and Ding, 1998). Belford et al. (1985) reported that waterlogging during jointing reduced yield through decreased grain number per spike, not via reduced tiller number. On the other hand, Araki et al. (2012) reported that waterlogging during jointing induces rapid leaf senescence in the grain filling period. So far, it has been reported that the important traits for waterlogging tolerance in plants are the formation of aerenchyma and
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Please cite this article in press as: Hayashi, T., et al., Maintained root length density contributes to the waterlogging tolerance in common wheat (Triticum aestivum L.). Field Crops Res. (2013), http://dx.doi.org/10.1016/j.fcr.2013.03.020
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24.0 109.5 74.0 115.0 125.5 188.0 240.0
2009–2010 2008–2009 2007–2008
90.0 26.5 52.0 152.0 198.5 211.5 228.5 110.5 36.5 62.0 86.5 29.5 128.0 210.0
2006–2007 2005–2006
33.0 49.5 124.5 117.5 104.5 205.0 221.0 9.2 9.3 11.0 13.2 15.6 20.6 18.1
2009–2010 2008–2009
9.1 9.8 11.8 15.5 20.4 18.7 18.6 8.0 9.4 12.9 16.6 18.8 18.7 15.7 7.7 9.6 13.1 15.5 18.3 20.6 19.1 8.1 9.4 10.4 15.0 15.5 15.4 16.4
2007–2008 2006–2007 2005–2006
7.6 4.6 7.0 9.1 13.3 18.7 23.9
2009–2010 2008–2009
8.0 5.3 7.3 9.5 15.4 19.9 23.3 8.0 5.1 4.0 10.4 15.3 19.6 22.4
2007–2008 2006–2007
7.6 6.1 7.7 9.0 14.0 19.0 23.1 3.4 3.8 5.5 7.8 13.0 18.7 23.3
2005–2006
the architecture of root system (Haque et al., 2012). Aerenchyma is a specialized plant tissue containing enlarged gas spaces and functions in aeration in plants (Armstrong, 1979; Armstrong and Armstrong, 1988; Mano and Omori, 2007). Root aerenchyma enhances gas exchange and supplies oxygen to the root tips from aerial part of plant tissues under hypoxic conditions in waterlogged soils (Shiono et al., 2011). The response to waterlogging in different wheat cultivars varies in terms of aerenchyma formation (Setter et al., 1999). Furthermore, the waterlogging tolerance measured as grain yield is correlated with increased aerenchyma formation (Setter and Waters, 2003). On the other hand, Haque et al. (2012) reported that the capacity to form aerenchyma in the seminal root is not sufficient for the expression of waterlogging tolerance in some Japanese wheat cultivars. In terms of root architecture, since the upper-layer soil contains higher concentrations of oxygen than the lower-layer one, plants with more shallow roots have better tolerance to waterlogged conditions (Oyanagi et al., 2004). These results indicate that maintaining the root respiration using aerenchyma or functional root architecture is important for the development of roots under wet conditions, which consequently contributes to greater yields under waterlogged conditions. However, only a few studies have been reported on the physiological function of root development in waterlogging tolerance and how it contributes to the better production of shoot dry matter and the resultant yield under waterlogged conditions. To identify genetic resources for waterlogging tolerance and use them for the breeding of wheat, it is important to determine the phenotypic differences in the waterlogging tolerance of wheat cultivars with wide genotypic variation. We selected Nishikazekomugi and Iwainodaichi as waterlogging-tolerant cultivars and UNICULM as a susceptible cultivar from 144 diverse wheat genotypes collected domestically as well as from overseas. The plants were subjected to waterlogging from jointing to maturity over five consecutive cropping seasons. By comparing the growth of roots and shoots and grain yield between waterlogging tolerant and susceptible cultivars, we show that greater root development is related to maintaining water uptake and the resultant photosynthesis and yield production in common wheat grown under waterlogged conditions.
2. Materials and methods
December January February March April May June
Precipitation (mm) Solar radiation (MJ m−2 d−1 ) Mean temperature (◦ C)
Table 1 Monthly means for mean air temperature, daily solar radiation and total precipitation during wheat cropping (December–June) from 2005/2006 to 2009/2010.
58.0 11.5 137.0 211.0 183.5 167.0 259.0
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2.1. Plant materials The five common wheat cultivars, Nishikazekomugi, Iwainodaichi, Shiroganekomugi, Norin 61 and UNICULM were used for the field experiments in this study (2006–2010). We used three wheat cultivars (Iwainodaichi, Norin 61, UNICULM) in 2006, three cultivars (Shiroganekomugi, Norin 61, UNICULM) in 2007, five cultivars (Nishikazekomugi, Iwainodaichi, Shiroganekomugi, Norin 61, UNICULM) in 2008 and three cultivars (Nishikazekomugi, Iwainodaichi, UNICULM) in 2009 and 2010. The cultivars used in this study were chosen from 144 wheat cultivars by screening under waterlogging treatments in the fields based on the relative growth and waterlogged conditions in comparison with well-drained control that have been performed from 1996 to 2005 (Yoshida et al., unpublished data). Norin 61, one of the leading cultivars for Japanese noodle flour in Japan, was used as a standard. Nishikazekomugi and Iwainodaichi were used as waterlogging tolerant cultivars. Shiroganekomugi was used as an intermediate waterlogging tolerant cultivar. Shiroganekomugi was also reported as a waterlogging tolerant cultivar with shallow root system (Oyanagi, 1994). UNICULM was used as a waterlogging susceptible cultivar.
Please cite this article in press as: Hayashi, T., et al., Maintained root length density contributes to the waterlogging tolerance in common wheat (Triticum aestivum L.). Field Crops Res. (2013), http://dx.doi.org/10.1016/j.fcr.2013.03.020
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Fig. 1. The photo of the field used for waterlogging treatment (a) and an irrigation channel (b). Arrows indicate the irrigation channels.
2.2. Experiment design
2.4. Root length density
We conducted a series of experiments at the experimental field in Aichi Agricultural Research Center (AARC; Aichi, Japan, 35◦ 16 N, 137◦ 07 E) from 2006 to 2010. Soil type of the field was andosol. Table 1 summarizes the climate data during the five wheat-growing seasons. Daily mean temperature, precipitation and total radiation was obtained from the dataset of the Nagoya Meteorological Station (9.6 km from the experimental site). The size of the fields for control and waterlogging was 80 m in length × 10 m in width and 100 m in length × 10 m in width, respectively. In 2006–2008, the seeds were drill-planted in rows (2.0 m in length and 0.2 m in width, 0.4 m apart) at a seeding rate of 240 seeds m−2 . In 2009 and 2010, one seed was planted per hill, and each row contained seven hills of a certain cultivar, which contained two border plants. Each cultivar was replicated five times, which were randomized. The sowing dates were 4th, 5th, 8th, 1st and 3rd of December in 2005, 2006, 2007, 2008 and 2009, respectively. A ditch was dug along both sides of long edges of the plot for waterlogging treatment, which was connected to the central drainage channels of the field (Fig. 1a). Twenty-four irrigation channels were set 3.9 m apart (arrows in Fig. 1). These were connected to the ditch so that the ground-water level could be adjusted by regulating the water level in the ditch. The waterlogging treatment was done by maintaining the ground-water level to 0–5 cm below the soil surface. The waterlogging treatment was imposed from the jointing stage till maturity (April 11–May 30 in 2006, April 9–May 30 in 2007, April 8–May 26 in 2008, April 13–June 1 in 2009, and April 9–May 31 in 2010). The harvest dates of 2006–2010 were June 24, June 25, July 2, June 28 and July 1, respectively. We applied 60 kg ha−1 of P2 O5 , 70 kg ha−1 of K2 O and 100 kg ha−1 of N basally. After the measurement of leaf water potential, stomatal conductance and photosynthetic rate, the plants were sampled for the analyses of grain yield, yield component and root development.
The soil cores (15 cm diameter, 30 cm deep) (one core per plot, five replicates) were taken using a stainless soil sampler and a 0–20 cm section from the ground surface was gently washed to collect roots on July 2 in 2008, June 28 in 2009 and July 1 in 2010. The roots were conserved in FAA solution (formalin:acetic acid:70% (v/v) ethanol = 1:1:18 by volume) until scanning. After removing the debris, the roots were stained in 0.25% (w/v) Coomassie Brilliant Blue R aqueous solution for 48 h. The stained roots were then rinsed with tap water and put on a plastic sheet. Digital images were then taken using Epson scanner (ES2200) at 300 dpi resolution. The root length was measured using a macro program developed by Kimura et al. (1999) and Kimura and Yamasaki (2001) on NIH image software version 1.62 as described previously (Kano-Nakata et al., 2011) and expressed as root length density (cm m−3 ).
2.3. Grain yield, shoot dry weight and whole grain ratio In 2006–2008, grain yield determination was conducted by harvesting each cultivar from an area of 1.2 m2 per plot in five rows. In 2009 and 2010, we harvested five samples per plot except borders in five rows. After air-drying for about three weeks, shoot dry weight was measured and the spikes were hand-threshed. After the grain moisture content was measured with a grain moisture tester, the grains were weighed for yield measurement. The whole grain ratio was calculated as the proportion of grains that were bigger than 2.2 mm in thickness.
2.5. Leaf water potential We determined water potential of the flag leaves (one leaf per plot, five replicates) in 2008–2010 by using leaf cutter psychrometer (J.R.D. Merrill Specialty Equipment, Logan, UT, USA), which had been calibrated with NaCl solution of a known molarity in advance. In preliminary measurements, we had confirmed the time required for the equilibrium, which was 4 h. After the equilibration, the leaf cutter psychrometer was connected to the microvoltmeter (model HR-33T, Wescor Inc., Logan, UT, USA). The measurement was carried out with psychometric method with a thermocouple cooling time of 20 s. Leaf water potential was measured five times (4, 11, 19, 25 and 34 d after the start of waterlogging treatment) in 2008, nine times (8, 11, 14, 17, 19, 22, 25, 27 and 31 d) in 2009, and six times (4, 11, 16, 19, 28 and 34 d) in 2010. 2.6. Stomatal conductance and photosynthetic rate We determined stomatal conductance and photosynthetic rate using the flag leaves (three leaves per plot, five replicates) seven times (4, 8, 11, 15, 19, 25 and 34 d after the start of waterlogging) in 2008, nine times (8, 11, 14, 17, 19, 22, 25, 27 and 31 d after the start of waterlogging) in 2009, and six times (4, 11, 16, 19, 28 and 34 d after the start of waterlogging) in 2010. The measurement was conducted at 8:00–13:00 h under clear conditions at PPFD of 1400 mol m−2 s−1 using a portable photosynthesis and transpiration measurement system (LI-6400, LI-COR, Lincoln, NE, USA). Leaf temperature and CO2 concentrations surrounding leaf was set at 28 ± 1.7 ◦ C and 400 mol mol−1 , respectively. Measurement duration averaged about 40–60 s. The leaf areas enclosed by chamber were 3.0–6.0 cm2 .
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Table 2 Percentage (W/C) of grain yield under waterlogged conditions in comparison to control among 5 cultivars from 2006 to 2010. The results of ANOVA for grain yield are also shown. Cultivars
Nishikazekomugi Iwainodaichi Shiroganekomugi Norin 61 UNICULM Treatment Cultivars Treatment × cultivars
Cultivars
W/C of grain yield (%) 2006
2007
2008
2009
2010
64 38
73 56
19 4
40 39 11
69 73 64 66 58
4
7
**
**
**
**
**
**
**
**
**
**
**
**
**
**
**
37
Table 3 Percentage (W/C) of whole grain ratio under waterlogged conditions in comparison to control among 5 cultivars from 2006 to 2010. The results of ANOVA for whole grain ratio are also shown. W/C of whole grain ratio (%) 2006 Nishikazekomugi Iwainodaichi Shiroganekomugi Norin 61 UNICULM Treatment Cultivars Treatment × cultivars
2007
2008
2009
2010
104 70
101 78
77 11
96 95 21
95 88 83 63 34
38
22
**
**
**
**
**
**
**
**
**
**
**
**
**
**
**
69
Data are means of 5 replicates. W/C (%), the percentage of the data under waterlogged conditions in comparison to control. ns, not significant at P = 0.05. ** P < 0.05.
Data are means of 5 replicates. W/C (%), the percentage of the data under waterlogged conditions in comparison to control. ns, not significant at P = 0.05. ** P < 0.05.
2.7. Data analysis
the cultivars except Nishikazekomugi. The percentage of the whole grain ratio under waterlogged conditions in comparison to control was the highest in Nishikazekomugi (95–104%), followed by Iwainodaichi (69–88%), and UNICULM (11–34%). The W/C of the whole grain ratio of Norin 61 and Shiroganekomugi was also higher than that of UNICULM. The effect of years and the interaction between years and cultivars on the whole grain ratio was found to be not significant (at the 5% level).
For statistical analysis of the data on leaf water potential, stomatal conductance and photosynthetic rate, we applied the repeated measures analysis for each environment using the PROC MIXED (SAS/STAT software) to test the effect of variety, time and their interaction. The Tukey’s test was used for mean comparison. To test the effect of environment and its interaction with variety and time, a combined repeated measures analysis was used. For data on grain yield, whole grain ratio and root length density, analysis for each year and environment was done using the mixed model with variety as fixed effect and replication as random effect, which was done using the PROC MIXED (SAS/STAT software). Comparison of cultivar means was done using the Tukey’s test. To test the effect of environment for each year, a combined analysis was done using the mixed model with environment, cultivar and their interaction as fixed effect and year, replication within year and environment, and the interaction of year with the other factors as random effects. To test the consistency of results over years, a combined analysis was done using the mixed model with environment, cultivar and their interaction as fixed effect and year, replication within year and environment, and the interaction of year with the other factors as random effects. 3. Results 3.1. Grain yield Table 2 shows the grain yield of five common wheat cultivars grown under control and waterlogged conditions. W/C (%) indicates the percentage of the data under waterlogged conditions in comparison to control. Generally, the grain yield of all the cultivars was decreased by the waterlogging treatment. The percentage of the grain yield under waterlogged conditions in comparison to control was the highest in Nishikazekomugi (64–73%), followed by Iwainodaichi (37–73%), and finally UNICULM (4–58%). The W/C of the grain yield of Norin 61 (one of the leading cultivars in Japan) and Shiroganekomugi was also higher than that of UNICULM. The effect of years and the interaction between years and cultivars on the grain yield was found to be not significant (at the 5% level). 3.2. Whole grain ratio Table 3 shows the whole grain ratio of five common wheat cultivars grown in control and waterlogged conditions. The whole grain ratio was decreased by the waterlogging treatment in all
3.3. Shoot dry weight Table 4 shows the shoot dry weight of five common wheat cultivars grown in control and waterlogged conditions in 2006–2008. Overall, the shoot dry weight was significantly decreased by the waterlogging treatment. The percentage of the shoot dry weight under waterlogged conditions in comparison to control was the highest in Nishikazekomugi (66% in 2008), followed by Iwainodaichi (33 and 63% in 2006 and 2008, respectively), Shiroganekomugi (45 and 41% in 2007 and 2008, respectively), Norin 61 (28–44%) and UNICULM (29–33%) under waterlogging. The effect of years and the interaction between years and cultivars on the shoot dry weight was found to be not significant (at the 5% level). 3.4. Relationship between the grain yield and shoot dry weight Fig. 2 shows the relationship between grain yield and shoot dry weight under control and waterlogged conditions in 2006–2008. The grain yield was positively correlated with the shoot dry weight Table 4 Percentage (W/C) of shoot dry weight under waterlogged conditions in comparison to control among 5 cultivars from 2006 to 2008. The results of ANOVA for shoot dry weight are also shown. Cultivars
W/C of shoot dry weight (%) 2006
Nishikazekomugi Iwainodaichi Shiroganekomugi Norin 61 UNICULM Treatment Cultivars Treatment × cultivars
2007
2008
28 29
45 44 32
66 63 41 41 33
**
**
**
**
**
**
**
**
**
33
Data are means of 5 replicates. W/C (%), the percentage of the data under waterlogged conditions in comparison to control. ns, not significant at P = 0.05. ** P < 0.05.
Please cite this article in press as: Hayashi, T., et al., Maintained root length density contributes to the waterlogging tolerance in common wheat (Triticum aestivum L.). Field Crops Res. (2013), http://dx.doi.org/10.1016/j.fcr.2013.03.020
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Fig. 2. Relationship between shoot dry weight and grain yield of Nishikazekomugi (), Iwainodaichi ( control and waterlogged conditions in 2006–2008. Control, r = 0.87**; waterlogging, r = 0.90**; **P < 0.01.
among the cultivars grown under both control and waterlogged conditions (r = 0.87 and 0.90, respectively, P < 0.01; Fig. 2). 3.5. Root length density In the experiment of 2008, the root length density of Nishikazekomugi, Iwainodaichi and Shiroganekomugi under waterlogged conditions was comparable to the control conditions (W/C was 106, 102 and 103%, respectively) (Table 5). However, Norin 61 and UNICULM showed decreased root length density under waterlogging in comparison to the control in 2008 (W/C was 82 and 76%, respectively). Nishikazekomugi, Iwainodaichi and UNICULM were used for the experiments in 2009 and 2010. The percentage of the root length density under waterlogged conditions in comparison to control was highest in Nishikazekomugi (82–87%), followed by Iwainodaichi (70–71%), and UNICULM (53–56%) (Table 5). The effect of years and the interaction between years and cultivars on the root length density was found to be not significant (at the 5% level). 3.6. Leaf water potential, stomatal conductance and photosynthetic rate Nishikazekomugi, Iwainodaichi and UNICULM were taken for the measurement of leaf water potential, stomatal conductance and photosynthetic rate in 2008 and 2010 as highly tolerant, Table 5 Percentage (W/C) of root length density under waterlogged conditions in comparison to control among 5 cultivars from 2008 to 2010. The results of ANOVA for root length density are also shown. Cultivars
Nishikazekomugi Iwainodaichi Shiroganekomugi Norin 61 UNICULM Treatment Cultivars Treatment × cultivars
W/C of root length density (%) 2008
2009
2010
106 102 103 82 76
87 70
82 71
53
56
**
**
**
**
**
**
**
**
**
Data are means of 5 replicates. W/C (%), the percentage of the data under waterlogged conditions in comparison to control. ns, not significant at P = 0.05. ** P < 0.05.
), Shiroganekomugi (
5
), Norin 61 (
) and UNICULM (䊉) under
moderately tolerant and susceptible to waterlogging, respectively, based on the result of grain yield and whole grain ratio (Tables 2 and 3). In the fields, root water uptake rate could not be directly measured. Instead, we measured the stomatal conductance to show the ability of roots for water uptake. Although the leaf water potential, stomatal conductance and photosynthetic rate in the flag leaf of all the common wheat cultivars were significantly decreased with aging under both control and waterlogged conditions, the plants grown under waterlogging showed more drastic reductions in comparison to the control (Figs. 3–5). For the experiment conducted in 2008, the leaf water potential was not significantly decreased by waterlogging in Nishikazekomugi and Iwainodaichi, however, UNICULM showed significant decrease under waterlogged conditions 25 d after the start of the treatment (Fig. 3). In the experiment of 2009, the leaf water potential was significantly decreased in Nishikazekomugi, Iwainodaichi and UNICULM 25 d, 22 d and 11 d after the start of the treatments, respectively. In 2010, the leaf water potential was significantly decreased by waterlogging in Nishikazekomugi, Iwainodaichi and UNICULM 19 d, 16 d and 11 d after the start of the treatments, respectively. In the experiment conducted in 2008, the stomatal conductance in Nishikazekomugi and UNICULM was decreased by waterlogging after 34 d and 15 d, respectively (Fig. 4). The stomatal conductance of Iwainodaichi under waterlogged conditions was decreased after 19 d from the start of waterlogging but recovered to the control level at 25 d, then decreased after 34 d in comparison to control. In 2009, the stomatal conductance of Nishikazekomugi under waterlogged conditions was decreased after 17 d from the start of waterlogging but recovered to the control level at 19 d, then decreased after 22 d in comparison to control. The stomatal conductance in Iwainodaichi and UNICULM was decreased by waterlogging after 19 d and 17 d, respectively. In 2010, the stomatal conductance in Nishikazekomugi, Iwainodaichi and UNICULM was decreased by waterlogging after 19 d, 19 d and 16 d, respectively. The photosynthetic rate was significantly decreased by waterlogging after 34 d in UNICULM but not in Nishikazekomugi and Iwainodaichi in 2008 (Fig. 5). In 2009, the photosynthetic rate of Nishikazekomugi under waterlogged conditions was decreased after 11 d from the start of waterlogging but recovered to the control level at 14 d, then decreased after 27 d in comparison to control. The photosynthetic rate in Iwainodaichi and UNICULM was decreased by waterlogging after 25 d and 14 d, respectively. In 2010, the photosynthetic rate in Nishikazekomugi, Iwainodaichi
Please cite this article in press as: Hayashi, T., et al., Maintained root length density contributes to the waterlogging tolerance in common wheat (Triticum aestivum L.). Field Crops Res. (2013), http://dx.doi.org/10.1016/j.fcr.2013.03.020
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Fig. 3. Leaf water potential of Nishikazekomugi, Iwainodaichi and UNICULM under control () and waterlogged (䊉) conditions in 2008–2010. Data are means of 5 replicates. ** indicates significant difference between the control and waterlogged conditions at each period (P < 0.01).
and UNICULM was decreased by waterlogging after 19 d, 16 d and 16 d, respectively. 3.7. Relationship between the stomatal conductance and root length density Fig. 6 indicates the relationship between stomatal conductance and root length density under control and waterlogged conditions in 2008–2010. The data on stomatal conductance at 15, 17 and 16 d after the start of waterlogging in 2008–2010, respectively (Fig. 4), were used for correlation analysis as these were days when stomatal conductance of waterlogging-susceptible UNICULM began to decrease by waterlogging. The stomatal conductance showed a positive correlation with the root length density among the cultivars grown under both control and waterlogged conditions (r = 0.67 and 0.83, respectively, P < 0.01). 4. Discussion The grain yield and whole grain yield were decreased in all the common wheat cultivars by the waterlogging treatments from the jointing stage till maturity in five years. However, the decrease of the relative grain yield under waterlogging was greater in UNICULM compared to Nishikazekomugi and Iwainodaichi, which indicates the genotypic variation of waterlogging tolerance. Although some wheat cultivar such as Brookton in Australia (Singh and Singh, 2003), Ducula-4 and Cucula-1 in Mexico, PF8442 in Brazil and Mikn Yang #11 and Zhen 7853 in China (Sayre et al., 1994) were reported to be tolerant to waterlogging, Nishikazekomugi and Iwainodaichi could be new waterlogging tolerant cultivars found within Japanese
cultivars. These cultivars will be useful for genetic analysis and breeding of waterlogging tolerance in Japanese cultivars since only few waterlogging tolerant cultivars has been reported. The relative whole grain ratio was greatly decreased in UNICULM, but not as much in Nishikazekomugi (Table 3), a tendency that was consistent with the data on the grain yield. This result indicates that the decrease of grain yield under waterlogging from the jointing stage until maturity was partly due to the decrease of the grain filling, which has also been reported in other wheat cultivars (Belford et al., 1985). From the results obtained, Nishikazekomugi and Iwainodaichi may be possible candidates for further breeding to improve the waterlogging tolerance from the jointing stage till maturity. The leaf water potential, stomatal conductance, and photosynthetic rate were examined in Nishikazekomugi, Iwainodaichi and UNICULM grown under both control and waterlogged conditions in 2008–2010. In 2008, the leaf water potential and photosynthetic rate were not decreased in Nishikazekomugi and Iwainodaichi under waterlogged conditions (Figs. 3 and 5). This result indicates that the waterlogging stress was not severe in comparison to that in 2009 and 2010, as shown by the result of grain yield (Table 2). However, UNICULM showed a decrease in all the parameters in 2008 (Figs. 3–5), which suggests that UNICULM is more susceptible to waterlogging treatments compared with Nishikazekomugi and Iwainodaichi. In the experiments conducted in 2009 and 2010, Iwainodaichi showed greater decrease in leaf water potential, stomatal conductance, and photosynthetic rate from earlier period compared with Nishikazekomugi (Figs. 3–5), which is consistent with the result of grain yield (Table 2). These results indicate that Nishikazekomugi
Please cite this article in press as: Hayashi, T., et al., Maintained root length density contributes to the waterlogging tolerance in common wheat (Triticum aestivum L.). Field Crops Res. (2013), http://dx.doi.org/10.1016/j.fcr.2013.03.020
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Fig. 4. Stomatal conductance of Nishikazekomugi, Iwainodaichi and UNICULM under control () and waterlogged (䊉) conditions in 2008–2010. Data are means of 5 replicates. ** indicates significant difference between the control and waterlogged conditions at each period (P < 0.01).
is the most tolerant to waterlogging treatments, followed by Iwainodaichi and UNICULM. It was also demonstrated that the senescence in the flag leaves, which was indicated by the decline of the photosynthetic rate, was accelerated by the waterlogging from the jointing stage till maturity (Fig. 4). The accelerated senescence under waterlogging is similar to abnormal early ripening that occurs in waterlogging-prone area (Hossain et al., 2011). Araki et al. (2012) also suggested that root injury by waterlogging at jointing induces rapid leaf senescence in the grain filling period, although they did not show any data on the root growth under waterlogging. Next, we found that the relative root length density was decreased greater in UNICULM, followed by Iwainodaichi and Nishikazekomugi under waterlogged conditions in comparison to control (Table 3). Because root length is an important factor that determines the size of contact with soil and thus the capability of water and nutrient uptake (Gowda et al., 2011), this result indicates that the greater root development under waterlogging is related to the waterlogging tolerance in Nishikazekomugi and Iwainodaichi. This is consistent with the results that leaf water potential was maintained higher in Nishikazekomugi and Iwainodaichi under waterlogging than in UNICULM. These indicate that the greater root development under waterlogging is involved in higher leaf water potential, and consequently stomatal conductance, photosynthetic rate and higher grain yield in wheat. Further study will need to be performed to determine the relationship between greater root development and higher stomatal conductance and photosynthetic rate in waterlogging-tolerant wheat cultivars by using near-isogenic lines with higher maintenance of root development under waterlogging.
The mechanism on how root development was maintained under waterlogging in Nishikazekomugi and Iwainodaichi remains unclear. When plants suffer by waterlogging, the roots become O2 deficient and growth finally stops (Jackson and Armstrong, 1999; Malik et al., 2003). Therefore, the formation of aerenchyma in roots is one of the important traits for maintaining root growth under waterlogging by supplying O2 to the root apex (Armstrong, 1971; Arikado, 1975; Colmer, 2003; Setter and Waters, 2003). We anticipated that waterlogging-tolerant cultivars may have an advantage for the formation of aerenchyma in the roots under waterlogging, which promotes root development. It was also reported that the enhanced lateral root formation contributes to maintaining high root length density and consequently to high drought tolerance in rice under water supply-limited conditions (Kano et al., 2011). We need to investigate how and which root traits such as aerenchyma formation and lateral root development are necessary for the maintained root length density in the waterlogging-tolerant wheat cultivars in further study. In addition, the water absorption ability in plants is defined by not only the root length but also the hydraulic conductance of roots. In this study, we showed that the maintained root length density is correlated with the waterlogging tolerance in wheat, although root hydraulic conductance was not determined. In a future study, it is needed to elucidate whether the hydraulic conductance in roots is also an important factor for waterlogging tolerance in wheat. In conclusion, we have found that the maintained root development is an important quantitative trait to maintain water uptake under waterlogged conditions, and is positively correlated with the leaf water potential, stomatal conductance and photosynthetic rate in the flag leaf of waterlogging-tolerant wheat cultivars. Therefore,
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Fig. 5. Photosynthetic rate of Nishikazekomugi, Iwainodaichi and UNICULM under control () and waterlogged (䊉) conditions in 2008–2010. Data are means of 5 replicates. ** indicates significant difference between the control and waterlogged conditions at each period (P < 0.01).
Fig. 6. Relationship between root length density and stomatal conductance of Nishikazekomugi (), Iwainodaichi ( ) and UNICULM (䊉) under control and waterlogged conditions in 2008–2010. The data on stomatal conductance at 15, 17 and 16 d after the start of waterlogging in 2008–2010, respectively (Fig. 4), were used for correlation analysis. Control, r = 0.67**; waterlogging, r = 0.83**; **P < 0.01.
greater root development is suggested to be involved in improving the grain yield in wheat plants under waterlogged conditions. It is interesting to note that the maintained root development is also a key trait for the adaptation in rice under progressive drought (Kano et al., 2011), drought to rewatering (Siopongco et al., 2005), transient waterlogging to drought and vice versa (Suralta et al., 2008a,b, 2010; Suralta and Yamauchi, 2008) and continuous cycle of alternate waterlogging to drought (Niones et al., 2012, 2013). Roots also produce signals in response to progressive drought, which regulates stomatal conductance, transpiration and shoot growth (Siopongco et al., 2008). These suggest that root development
plasticity is essential to tolerate water-limited environment caused by drought or waterlogging-induced root injury. The waterloggingtolerant wheat cultivars found in this study will be available to elucidate the quantitative mechanism of the plastic development of roots under waterlogging tolerance in wheat. Acknowledgements The authors would like to thank Ms. Violeta Bartolome of International Rice Research Institute for assistance in statistical analysis and Dr. Joyce A. Cartagena of Nagoya University for editing and
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reviewing the manuscript. This work was partially supported by JSPS KAKENHI Grant Number 22380013 (to A.Y.). References Araki, H., Hamada, A., Hossain, M.A., Takahashi, T., 2012. Waterlogging at jointing and/or after anthesis in wheat induces early leaf senescence and impairs grain filling. Field Crops Res. 137, 27–36. Arikado, H., 1975. Ventilating System and Tolerance to Waterlogging in Crop Plants. Oriental Print, Kawagei, Mie (in Japanese). Armstrong, W., 1971. Radial oxygen losses from intact rice roots as affected by distance from the apex, respiration, and waterlogging. Physiol. Plant. 25, 192–197. Armstrong, W., 1979. Aeration in higher plants. Adv. Bot. Res. 7, 226–332. Armstrong, J., Armstrong, W., 1988. Phragmites australis – a preliminary study of soiloxidizing sites and internal gas transport pathways. New Phytol. 108, 373–382. Belford, R.K., 1981. Response of winter wheat to prolonged waterlogging under outdoor conditions. J. Agric. Sci. 97, 557–568. Belford, R.K., Cannell, R.Q., Thomson, R.J., 1985. Effects of single and multiple waterlogging on the growth and yield of winter wheat on a clay soil. J. Sci. Food Agric. 36, 142–156. Boyer, J.S., 1982. Plant productivity and environment. Science 218, 443–448. Cannell, R.Q., Belford, R.K., 1980. Effects of waterlogging at different stages of development on the growth and yield of winter oilseed rape (Brassica napus L.). J. Sci. Food Agric. 31, 963–965. Cannell, R.Q., Belford, R.K., Gales, K., Thomson, R.J., Webster, C.P., 1984. Effects of waterlogging and drought on winter wheat and winter barley grown on a clay and a sandy loam soil. Plant Soil 80, 53–66. Colmer, T.D., 2003. Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deepwater rice (Oryza sativa L.). Ann. Bot. 91, 301–309. Colmer, T.D., Voesenek, L.A.C.J., 2009. Flooding tolerance: suites of plant traits in variable environments. Funct. Plant Biol. 36, 665–681. FAO, 2009. Agribusiness Handbook: Wheat Flour. http://www.fao.org/docrep/ 012/al376e/al376e.pdf Gowda, W.R.P., Henry, A., Yamauchi, A., Shashidhar, H.E., Serraj, R., 2011. Root biology and genetic improvement for drought avoidance in rice. Field Crops Res. 122, 1–13. Haque, M.D., Oyanagi, A., Kawaguchi, K., 2012. Aerenchyma formation in the seminal roots of Japanese wheat cultivars in relation to growth under waterlogged conditions. Plant Prod. Sci. 15, 164–173. Hossain, M.A., Araki, H., Takahashi, T., 2011. Poor grain filling induced by waterlogging is similar to that in abnormal early ripening in wheat in Western Japan. Field Crops Res. 123, 100–108. Jackson, M.B., Armstrong, W., 1999. Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biol. 1, 274–287. Kano, M., Inukai, Y., Kitano, H., Yamauchi, A., 2011. Root plasticity as the key root trait for adaptation to various intensities of drought stress in rice. Plant Soil 342, 117–128. Kano-Nakata, M., Inukai, Y., Wade, L.J., Siopongco, J.D.L.C., Yamauchi, A., 2011. Root development, water uptake, and shoot dry matter production under water deficit conditions in two CSSLs of rice: functional roles of root plasticity. Plant Prod. Sci. 14, 307–317. Kimura, K., Kikuchi, S., Yamasaki, S., 1999. Accurate root length measurement by image analysis. Plant Soil 216, 117–127. Kimura, K., Yamasaki, S., 2001. Root length and diameter measurement using NIH Image: application of the line-intercept principle for diameter estimation. Plant Soil 234, 37–46. Malik, A.I., Colmer, T.D., Lambers, H., Setter, T.L., Schortemeyer, M., 2002. Short-term waterlogging has long-term effects on the growth and physiology of wheat. New Phytol. 153, 225–236.
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Maintained root length density contributes to the waterlogging tolerance in common wheat (Triticum aestivum L.) Tomohito Hayashi a , Tomofumi Yoshida b , Kiyoshi Fujii b,c , Shiro Mitsuya a , Takako Tsuji b , Yurie Okada a , Eriko Hayashi a , Akira Yamauchi a,∗ a
Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan Aichi Prefecture Agricultural Research Center, 1-1, Aza-Sagamine, Oaza-Yazako, Nagakute-cho, Aichi-gun 480-1193, Japan c Agricultural Production Division, Aichi Prefectural Government, 3-1-2, Sannomaru, Naka-ku, Nagoya 460-8501, Japan b
a r t i c l e
i n f o
Article history: Received 31 October 2012 Received in revised form 25 March 2013 Accepted 30 March 2013 Keywords: Common wheat Triticum aestivum L. Grain yield Root length density Waterlogging
a b s t r a c t Waterlogging stress substantially reduces the growth and yield of common wheat (Triticum aestivum L.). Limited root development due to decreased availability of oxygen in roots is the major growth-limiting factor for plants under waterlogged conditions. In this study, we have determined whether a maintained root length density can be one of the important traits for waterlogging tolerance to maintain the shoot growth and grain yield, using waterlogging-tolerant and -susceptible wheat cultivars. This study was carried out over five consecutive cropping seasons (from 2006 to 2010), and the wheat plants were exposed to waterlogging from jointing stage to maturity. The waterlogging-tolerant cultivars Nishikazekomugi and Iwainodaichi showed higher relative grain yield and whole grain ratio under waterlogged conditions than the susceptible UNICULM. The waterlogging-tolerant cultivars maintained higher leaf water potential, stomatal conductance and photosynthetic rate under waterlogged conditions than the susceptible one, which was consistent with the higher relative root length density in the tolerant cultivars. These results indicate that maintained root length density is related to maintaining water uptake and the resultant photosynthesis and yield production in common wheat grown under waterlogged conditions. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Common wheat (Triticum aestivum) is an important staple crop plant together with rice and maize, and its production reached 610 million tons in 2007 (FAO, 2009). Wheat plants are mainly grown where annual precipitation is around 600–700 mm. Waterlogging is one of the important constraints that reduce the productivity of wheat in Japan, since the annual precipitation is greater than 1000 mm. In addition, wheat is generally cultivated in drained paddy fields that have been converted from paddy field to mitigate the problem of rice overproduction. Large-scale waterlogging in wheat also occurs in irrigated rice–wheat rotation systems in south and east Asia where wheat is cultivated in the fields that have top soil compaction for rice cultivation in flooding conditions (Samad et al., 2001). In the US, more than 10 million ha is affected by excess
∗ Corresponding author. Tel.: +81 52 789 4022; fax: +81 52 789 4022. E-mail addresses: [email protected] (T. Hayashi), tomofumi [email protected] (T. Yoshida), kiyoshi [email protected] (K. Fujii), [email protected] (S. Mitsuya), takako [email protected] (T. Tsuji), [email protected] (A. Yamauchi).
water conditions, which is equivalent to 12% of the total cultivated land (Boyer, 1982). Therefore, the improvement of waterlogging tolerance is an important target to increase and stabilize wheat production. When plants are exposed to waterlogged conditions, the availability of oxygen in the rhizosphere becomes limited (Ponnamperuma, 1972). Because oxygen is necessary for the respiration in roots, oxygen deficiency caused by waterlogging affects root growth and consequently reduces the shoot growth and yield (Malik et al., 2002; Colmer and Voesenek, 2009). The impact of waterlogging on the plant growth varies with different developmental stages. Waterlogging during the vegetative stage reduces grain yield due to a decrease in tiller number (Cannell and Belford, 1980; Belford, 1981; Cannell et al., 1984; Sharma and Swarup, 1988; Musgrave, 1994; Musgrave and Ding, 1998). Belford et al. (1985) reported that waterlogging during jointing reduced yield through decreased grain number per spike, not via reduced tiller number. On the other hand, Araki et al. (2012) reported that waterlogging during jointing induces rapid leaf senescence in the grain filling period. So far, it has been reported that the important traits for waterlogging tolerance in plants are the formation of aerenchyma and
0378-4290/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.fcr.2013.03.020
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24.0 109.5 74.0 115.0 125.5 188.0 240.0
2009–2010 2008–2009 2007–2008
90.0 26.5 52.0 152.0 198.5 211.5 228.5 110.5 36.5 62.0 86.5 29.5 128.0 210.0
2006–2007 2005–2006
33.0 49.5 124.5 117.5 104.5 205.0 221.0 9.2 9.3 11.0 13.2 15.6 20.6 18.1
2009–2010 2008–2009
9.1 9.8 11.8 15.5 20.4 18.7 18.6 8.0 9.4 12.9 16.6 18.8 18.7 15.7 7.7 9.6 13.1 15.5 18.3 20.6 19.1 8.1 9.4 10.4 15.0 15.5 15.4 16.4
2007–2008 2006–2007 2005–2006
7.6 4.6 7.0 9.1 13.3 18.7 23.9
2009–2010 2008–2009
8.0 5.3 7.3 9.5 15.4 19.9 23.3 8.0 5.1 4.0 10.4 15.3 19.6 22.4
2007–2008 2006–2007
7.6 6.1 7.7 9.0 14.0 19.0 23.1 3.4 3.8 5.5 7.8 13.0 18.7 23.3
2005–2006
the architecture of root system (Haque et al., 2012). Aerenchyma is a specialized plant tissue containing enlarged gas spaces and functions in aeration in plants (Armstrong, 1979; Armstrong and Armstrong, 1988; Mano and Omori, 2007). Root aerenchyma enhances gas exchange and supplies oxygen to the root tips from aerial part of plant tissues under hypoxic conditions in waterlogged soils (Shiono et al., 2011). The response to waterlogging in different wheat cultivars varies in terms of aerenchyma formation (Setter et al., 1999). Furthermore, the waterlogging tolerance measured as grain yield is correlated with increased aerenchyma formation (Setter and Waters, 2003). On the other hand, Haque et al. (2012) reported that the capacity to form aerenchyma in the seminal root is not sufficient for the expression of waterlogging tolerance in some Japanese wheat cultivars. In terms of root architecture, since the upper-layer soil contains higher concentrations of oxygen than the lower-layer one, plants with more shallow roots have better tolerance to waterlogged conditions (Oyanagi et al., 2004). These results indicate that maintaining the root respiration using aerenchyma or functional root architecture is important for the development of roots under wet conditions, which consequently contributes to greater yields under waterlogged conditions. However, only a few studies have been reported on the physiological function of root development in waterlogging tolerance and how it contributes to the better production of shoot dry matter and the resultant yield under waterlogged conditions. To identify genetic resources for waterlogging tolerance and use them for the breeding of wheat, it is important to determine the phenotypic differences in the waterlogging tolerance of wheat cultivars with wide genotypic variation. We selected Nishikazekomugi and Iwainodaichi as waterlogging-tolerant cultivars and UNICULM as a susceptible cultivar from 144 diverse wheat genotypes collected domestically as well as from overseas. The plants were subjected to waterlogging from jointing to maturity over five consecutive cropping seasons. By comparing the growth of roots and shoots and grain yield between waterlogging tolerant and susceptible cultivars, we show that greater root development is related to maintaining water uptake and the resultant photosynthesis and yield production in common wheat grown under waterlogged conditions.
2. Materials and methods
December January February March April May June
Precipitation (mm) Solar radiation (MJ m−2 d−1 ) Mean temperature (◦ C)
Table 1 Monthly means for mean air temperature, daily solar radiation and total precipitation during wheat cropping (December–June) from 2005/2006 to 2009/2010.
58.0 11.5 137.0 211.0 183.5 167.0 259.0
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2.1. Plant materials The five common wheat cultivars, Nishikazekomugi, Iwainodaichi, Shiroganekomugi, Norin 61 and UNICULM were used for the field experiments in this study (2006–2010). We used three wheat cultivars (Iwainodaichi, Norin 61, UNICULM) in 2006, three cultivars (Shiroganekomugi, Norin 61, UNICULM) in 2007, five cultivars (Nishikazekomugi, Iwainodaichi, Shiroganekomugi, Norin 61, UNICULM) in 2008 and three cultivars (Nishikazekomugi, Iwainodaichi, UNICULM) in 2009 and 2010. The cultivars used in this study were chosen from 144 wheat cultivars by screening under waterlogging treatments in the fields based on the relative growth and waterlogged conditions in comparison with well-drained control that have been performed from 1996 to 2005 (Yoshida et al., unpublished data). Norin 61, one of the leading cultivars for Japanese noodle flour in Japan, was used as a standard. Nishikazekomugi and Iwainodaichi were used as waterlogging tolerant cultivars. Shiroganekomugi was used as an intermediate waterlogging tolerant cultivar. Shiroganekomugi was also reported as a waterlogging tolerant cultivar with shallow root system (Oyanagi, 1994). UNICULM was used as a waterlogging susceptible cultivar.
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Fig. 1. The photo of the field used for waterlogging treatment (a) and an irrigation channel (b). Arrows indicate the irrigation channels.
2.2. Experiment design
2.4. Root length density
We conducted a series of experiments at the experimental field in Aichi Agricultural Research Center (AARC; Aichi, Japan, 35◦ 16 N, 137◦ 07 E) from 2006 to 2010. Soil type of the field was andosol. Table 1 summarizes the climate data during the five wheat-growing seasons. Daily mean temperature, precipitation and total radiation was obtained from the dataset of the Nagoya Meteorological Station (9.6 km from the experimental site). The size of the fields for control and waterlogging was 80 m in length × 10 m in width and 100 m in length × 10 m in width, respectively. In 2006–2008, the seeds were drill-planted in rows (2.0 m in length and 0.2 m in width, 0.4 m apart) at a seeding rate of 240 seeds m−2 . In 2009 and 2010, one seed was planted per hill, and each row contained seven hills of a certain cultivar, which contained two border plants. Each cultivar was replicated five times, which were randomized. The sowing dates were 4th, 5th, 8th, 1st and 3rd of December in 2005, 2006, 2007, 2008 and 2009, respectively. A ditch was dug along both sides of long edges of the plot for waterlogging treatment, which was connected to the central drainage channels of the field (Fig. 1a). Twenty-four irrigation channels were set 3.9 m apart (arrows in Fig. 1). These were connected to the ditch so that the ground-water level could be adjusted by regulating the water level in the ditch. The waterlogging treatment was done by maintaining the ground-water level to 0–5 cm below the soil surface. The waterlogging treatment was imposed from the jointing stage till maturity (April 11–May 30 in 2006, April 9–May 30 in 2007, April 8–May 26 in 2008, April 13–June 1 in 2009, and April 9–May 31 in 2010). The harvest dates of 2006–2010 were June 24, June 25, July 2, June 28 and July 1, respectively. We applied 60 kg ha−1 of P2 O5 , 70 kg ha−1 of K2 O and 100 kg ha−1 of N basally. After the measurement of leaf water potential, stomatal conductance and photosynthetic rate, the plants were sampled for the analyses of grain yield, yield component and root development.
The soil cores (15 cm diameter, 30 cm deep) (one core per plot, five replicates) were taken using a stainless soil sampler and a 0–20 cm section from the ground surface was gently washed to collect roots on July 2 in 2008, June 28 in 2009 and July 1 in 2010. The roots were conserved in FAA solution (formalin:acetic acid:70% (v/v) ethanol = 1:1:18 by volume) until scanning. After removing the debris, the roots were stained in 0.25% (w/v) Coomassie Brilliant Blue R aqueous solution for 48 h. The stained roots were then rinsed with tap water and put on a plastic sheet. Digital images were then taken using Epson scanner (ES2200) at 300 dpi resolution. The root length was measured using a macro program developed by Kimura et al. (1999) and Kimura and Yamasaki (2001) on NIH image software version 1.62 as described previously (Kano-Nakata et al., 2011) and expressed as root length density (cm m−3 ).
2.3. Grain yield, shoot dry weight and whole grain ratio In 2006–2008, grain yield determination was conducted by harvesting each cultivar from an area of 1.2 m2 per plot in five rows. In 2009 and 2010, we harvested five samples per plot except borders in five rows. After air-drying for about three weeks, shoot dry weight was measured and the spikes were hand-threshed. After the grain moisture content was measured with a grain moisture tester, the grains were weighed for yield measurement. The whole grain ratio was calculated as the proportion of grains that were bigger than 2.2 mm in thickness.
2.5. Leaf water potential We determined water potential of the flag leaves (one leaf per plot, five replicates) in 2008–2010 by using leaf cutter psychrometer (J.R.D. Merrill Specialty Equipment, Logan, UT, USA), which had been calibrated with NaCl solution of a known molarity in advance. In preliminary measurements, we had confirmed the time required for the equilibrium, which was 4 h. After the equilibration, the leaf cutter psychrometer was connected to the microvoltmeter (model HR-33T, Wescor Inc., Logan, UT, USA). The measurement was carried out with psychometric method with a thermocouple cooling time of 20 s. Leaf water potential was measured five times (4, 11, 19, 25 and 34 d after the start of waterlogging treatment) in 2008, nine times (8, 11, 14, 17, 19, 22, 25, 27 and 31 d) in 2009, and six times (4, 11, 16, 19, 28 and 34 d) in 2010. 2.6. Stomatal conductance and photosynthetic rate We determined stomatal conductance and photosynthetic rate using the flag leaves (three leaves per plot, five replicates) seven times (4, 8, 11, 15, 19, 25 and 34 d after the start of waterlogging) in 2008, nine times (8, 11, 14, 17, 19, 22, 25, 27 and 31 d after the start of waterlogging) in 2009, and six times (4, 11, 16, 19, 28 and 34 d after the start of waterlogging) in 2010. The measurement was conducted at 8:00–13:00 h under clear conditions at PPFD of 1400 mol m−2 s−1 using a portable photosynthesis and transpiration measurement system (LI-6400, LI-COR, Lincoln, NE, USA). Leaf temperature and CO2 concentrations surrounding leaf was set at 28 ± 1.7 ◦ C and 400 mol mol−1 , respectively. Measurement duration averaged about 40–60 s. The leaf areas enclosed by chamber were 3.0–6.0 cm2 .
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Table 2 Percentage (W/C) of grain yield under waterlogged conditions in comparison to control among 5 cultivars from 2006 to 2010. The results of ANOVA for grain yield are also shown. Cultivars
Nishikazekomugi Iwainodaichi Shiroganekomugi Norin 61 UNICULM Treatment Cultivars Treatment × cultivars
Cultivars
W/C of grain yield (%) 2006
2007
2008
2009
2010
64 38
73 56
19 4
40 39 11
69 73 64 66 58
4
7
**
**
**
**
**
**
**
**
**
**
**
**
**
**
**
37
Table 3 Percentage (W/C) of whole grain ratio under waterlogged conditions in comparison to control among 5 cultivars from 2006 to 2010. The results of ANOVA for whole grain ratio are also shown. W/C of whole grain ratio (%) 2006 Nishikazekomugi Iwainodaichi Shiroganekomugi Norin 61 UNICULM Treatment Cultivars Treatment × cultivars
2007
2008
2009
2010
104 70
101 78
77 11
96 95 21
95 88 83 63 34
38
22
**
**
**
**
**
**
**
**
**
**
**
**
**
**
**
69
Data are means of 5 replicates. W/C (%), the percentage of the data under waterlogged conditions in comparison to control. ns, not significant at P = 0.05. ** P < 0.05.
Data are means of 5 replicates. W/C (%), the percentage of the data under waterlogged conditions in comparison to control. ns, not significant at P = 0.05. ** P < 0.05.
2.7. Data analysis
the cultivars except Nishikazekomugi. The percentage of the whole grain ratio under waterlogged conditions in comparison to control was the highest in Nishikazekomugi (95–104%), followed by Iwainodaichi (69–88%), and UNICULM (11–34%). The W/C of the whole grain ratio of Norin 61 and Shiroganekomugi was also higher than that of UNICULM. The effect of years and the interaction between years and cultivars on the whole grain ratio was found to be not significant (at the 5% level).
For statistical analysis of the data on leaf water potential, stomatal conductance and photosynthetic rate, we applied the repeated measures analysis for each environment using the PROC MIXED (SAS/STAT software) to test the effect of variety, time and their interaction. The Tukey’s test was used for mean comparison. To test the effect of environment and its interaction with variety and time, a combined repeated measures analysis was used. For data on grain yield, whole grain ratio and root length density, analysis for each year and environment was done using the mixed model with variety as fixed effect and replication as random effect, which was done using the PROC MIXED (SAS/STAT software). Comparison of cultivar means was done using the Tukey’s test. To test the effect of environment for each year, a combined analysis was done using the mixed model with environment, cultivar and their interaction as fixed effect and year, replication within year and environment, and the interaction of year with the other factors as random effects. To test the consistency of results over years, a combined analysis was done using the mixed model with environment, cultivar and their interaction as fixed effect and year, replication within year and environment, and the interaction of year with the other factors as random effects. 3. Results 3.1. Grain yield Table 2 shows the grain yield of five common wheat cultivars grown under control and waterlogged conditions. W/C (%) indicates the percentage of the data under waterlogged conditions in comparison to control. Generally, the grain yield of all the cultivars was decreased by the waterlogging treatment. The percentage of the grain yield under waterlogged conditions in comparison to control was the highest in Nishikazekomugi (64–73%), followed by Iwainodaichi (37–73%), and finally UNICULM (4–58%). The W/C of the grain yield of Norin 61 (one of the leading cultivars in Japan) and Shiroganekomugi was also higher than that of UNICULM. The effect of years and the interaction between years and cultivars on the grain yield was found to be not significant (at the 5% level). 3.2. Whole grain ratio Table 3 shows the whole grain ratio of five common wheat cultivars grown in control and waterlogged conditions. The whole grain ratio was decreased by the waterlogging treatment in all
3.3. Shoot dry weight Table 4 shows the shoot dry weight of five common wheat cultivars grown in control and waterlogged conditions in 2006–2008. Overall, the shoot dry weight was significantly decreased by the waterlogging treatment. The percentage of the shoot dry weight under waterlogged conditions in comparison to control was the highest in Nishikazekomugi (66% in 2008), followed by Iwainodaichi (33 and 63% in 2006 and 2008, respectively), Shiroganekomugi (45 and 41% in 2007 and 2008, respectively), Norin 61 (28–44%) and UNICULM (29–33%) under waterlogging. The effect of years and the interaction between years and cultivars on the shoot dry weight was found to be not significant (at the 5% level). 3.4. Relationship between the grain yield and shoot dry weight Fig. 2 shows the relationship between grain yield and shoot dry weight under control and waterlogged conditions in 2006–2008. The grain yield was positively correlated with the shoot dry weight Table 4 Percentage (W/C) of shoot dry weight under waterlogged conditions in comparison to control among 5 cultivars from 2006 to 2008. The results of ANOVA for shoot dry weight are also shown. Cultivars
W/C of shoot dry weight (%) 2006
Nishikazekomugi Iwainodaichi Shiroganekomugi Norin 61 UNICULM Treatment Cultivars Treatment × cultivars
2007
2008
28 29
45 44 32
66 63 41 41 33
**
**
**
**
**
**
**
**
**
33
Data are means of 5 replicates. W/C (%), the percentage of the data under waterlogged conditions in comparison to control. ns, not significant at P = 0.05. ** P < 0.05.
Please cite this article in press as: Hayashi, T., et al., Maintained root length density contributes to the waterlogging tolerance in common wheat (Triticum aestivum L.). Field Crops Res. (2013), http://dx.doi.org/10.1016/j.fcr.2013.03.020
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Fig. 2. Relationship between shoot dry weight and grain yield of Nishikazekomugi (), Iwainodaichi ( control and waterlogged conditions in 2006–2008. Control, r = 0.87**; waterlogging, r = 0.90**; **P < 0.01.
among the cultivars grown under both control and waterlogged conditions (r = 0.87 and 0.90, respectively, P < 0.01; Fig. 2). 3.5. Root length density In the experiment of 2008, the root length density of Nishikazekomugi, Iwainodaichi and Shiroganekomugi under waterlogged conditions was comparable to the control conditions (W/C was 106, 102 and 103%, respectively) (Table 5). However, Norin 61 and UNICULM showed decreased root length density under waterlogging in comparison to the control in 2008 (W/C was 82 and 76%, respectively). Nishikazekomugi, Iwainodaichi and UNICULM were used for the experiments in 2009 and 2010. The percentage of the root length density under waterlogged conditions in comparison to control was highest in Nishikazekomugi (82–87%), followed by Iwainodaichi (70–71%), and UNICULM (53–56%) (Table 5). The effect of years and the interaction between years and cultivars on the root length density was found to be not significant (at the 5% level). 3.6. Leaf water potential, stomatal conductance and photosynthetic rate Nishikazekomugi, Iwainodaichi and UNICULM were taken for the measurement of leaf water potential, stomatal conductance and photosynthetic rate in 2008 and 2010 as highly tolerant, Table 5 Percentage (W/C) of root length density under waterlogged conditions in comparison to control among 5 cultivars from 2008 to 2010. The results of ANOVA for root length density are also shown. Cultivars
Nishikazekomugi Iwainodaichi Shiroganekomugi Norin 61 UNICULM Treatment Cultivars Treatment × cultivars
W/C of root length density (%) 2008
2009
2010
106 102 103 82 76
87 70
82 71
53
56
**
**
**
**
**
**
**
**
**
Data are means of 5 replicates. W/C (%), the percentage of the data under waterlogged conditions in comparison to control. ns, not significant at P = 0.05. ** P < 0.05.
), Shiroganekomugi (
5
), Norin 61 (
) and UNICULM (䊉) under
moderately tolerant and susceptible to waterlogging, respectively, based on the result of grain yield and whole grain ratio (Tables 2 and 3). In the fields, root water uptake rate could not be directly measured. Instead, we measured the stomatal conductance to show the ability of roots for water uptake. Although the leaf water potential, stomatal conductance and photosynthetic rate in the flag leaf of all the common wheat cultivars were significantly decreased with aging under both control and waterlogged conditions, the plants grown under waterlogging showed more drastic reductions in comparison to the control (Figs. 3–5). For the experiment conducted in 2008, the leaf water potential was not significantly decreased by waterlogging in Nishikazekomugi and Iwainodaichi, however, UNICULM showed significant decrease under waterlogged conditions 25 d after the start of the treatment (Fig. 3). In the experiment of 2009, the leaf water potential was significantly decreased in Nishikazekomugi, Iwainodaichi and UNICULM 25 d, 22 d and 11 d after the start of the treatments, respectively. In 2010, the leaf water potential was significantly decreased by waterlogging in Nishikazekomugi, Iwainodaichi and UNICULM 19 d, 16 d and 11 d after the start of the treatments, respectively. In the experiment conducted in 2008, the stomatal conductance in Nishikazekomugi and UNICULM was decreased by waterlogging after 34 d and 15 d, respectively (Fig. 4). The stomatal conductance of Iwainodaichi under waterlogged conditions was decreased after 19 d from the start of waterlogging but recovered to the control level at 25 d, then decreased after 34 d in comparison to control. In 2009, the stomatal conductance of Nishikazekomugi under waterlogged conditions was decreased after 17 d from the start of waterlogging but recovered to the control level at 19 d, then decreased after 22 d in comparison to control. The stomatal conductance in Iwainodaichi and UNICULM was decreased by waterlogging after 19 d and 17 d, respectively. In 2010, the stomatal conductance in Nishikazekomugi, Iwainodaichi and UNICULM was decreased by waterlogging after 19 d, 19 d and 16 d, respectively. The photosynthetic rate was significantly decreased by waterlogging after 34 d in UNICULM but not in Nishikazekomugi and Iwainodaichi in 2008 (Fig. 5). In 2009, the photosynthetic rate of Nishikazekomugi under waterlogged conditions was decreased after 11 d from the start of waterlogging but recovered to the control level at 14 d, then decreased after 27 d in comparison to control. The photosynthetic rate in Iwainodaichi and UNICULM was decreased by waterlogging after 25 d and 14 d, respectively. In 2010, the photosynthetic rate in Nishikazekomugi, Iwainodaichi
Please cite this article in press as: Hayashi, T., et al., Maintained root length density contributes to the waterlogging tolerance in common wheat (Triticum aestivum L.). Field Crops Res. (2013), http://dx.doi.org/10.1016/j.fcr.2013.03.020
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Fig. 3. Leaf water potential of Nishikazekomugi, Iwainodaichi and UNICULM under control () and waterlogged (䊉) conditions in 2008–2010. Data are means of 5 replicates. ** indicates significant difference between the control and waterlogged conditions at each period (P < 0.01).
and UNICULM was decreased by waterlogging after 19 d, 16 d and 16 d, respectively. 3.7. Relationship between the stomatal conductance and root length density Fig. 6 indicates the relationship between stomatal conductance and root length density under control and waterlogged conditions in 2008–2010. The data on stomatal conductance at 15, 17 and 16 d after the start of waterlogging in 2008–2010, respectively (Fig. 4), were used for correlation analysis as these were days when stomatal conductance of waterlogging-susceptible UNICULM began to decrease by waterlogging. The stomatal conductance showed a positive correlation with the root length density among the cultivars grown under both control and waterlogged conditions (r = 0.67 and 0.83, respectively, P < 0.01). 4. Discussion The grain yield and whole grain yield were decreased in all the common wheat cultivars by the waterlogging treatments from the jointing stage till maturity in five years. However, the decrease of the relative grain yield under waterlogging was greater in UNICULM compared to Nishikazekomugi and Iwainodaichi, which indicates the genotypic variation of waterlogging tolerance. Although some wheat cultivar such as Brookton in Australia (Singh and Singh, 2003), Ducula-4 and Cucula-1 in Mexico, PF8442 in Brazil and Mikn Yang #11 and Zhen 7853 in China (Sayre et al., 1994) were reported to be tolerant to waterlogging, Nishikazekomugi and Iwainodaichi could be new waterlogging tolerant cultivars found within Japanese
cultivars. These cultivars will be useful for genetic analysis and breeding of waterlogging tolerance in Japanese cultivars since only few waterlogging tolerant cultivars has been reported. The relative whole grain ratio was greatly decreased in UNICULM, but not as much in Nishikazekomugi (Table 3), a tendency that was consistent with the data on the grain yield. This result indicates that the decrease of grain yield under waterlogging from the jointing stage until maturity was partly due to the decrease of the grain filling, which has also been reported in other wheat cultivars (Belford et al., 1985). From the results obtained, Nishikazekomugi and Iwainodaichi may be possible candidates for further breeding to improve the waterlogging tolerance from the jointing stage till maturity. The leaf water potential, stomatal conductance, and photosynthetic rate were examined in Nishikazekomugi, Iwainodaichi and UNICULM grown under both control and waterlogged conditions in 2008–2010. In 2008, the leaf water potential and photosynthetic rate were not decreased in Nishikazekomugi and Iwainodaichi under waterlogged conditions (Figs. 3 and 5). This result indicates that the waterlogging stress was not severe in comparison to that in 2009 and 2010, as shown by the result of grain yield (Table 2). However, UNICULM showed a decrease in all the parameters in 2008 (Figs. 3–5), which suggests that UNICULM is more susceptible to waterlogging treatments compared with Nishikazekomugi and Iwainodaichi. In the experiments conducted in 2009 and 2010, Iwainodaichi showed greater decrease in leaf water potential, stomatal conductance, and photosynthetic rate from earlier period compared with Nishikazekomugi (Figs. 3–5), which is consistent with the result of grain yield (Table 2). These results indicate that Nishikazekomugi
Please cite this article in press as: Hayashi, T., et al., Maintained root length density contributes to the waterlogging tolerance in common wheat (Triticum aestivum L.). Field Crops Res. (2013), http://dx.doi.org/10.1016/j.fcr.2013.03.020
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Fig. 4. Stomatal conductance of Nishikazekomugi, Iwainodaichi and UNICULM under control () and waterlogged (䊉) conditions in 2008–2010. Data are means of 5 replicates. ** indicates significant difference between the control and waterlogged conditions at each period (P < 0.01).
is the most tolerant to waterlogging treatments, followed by Iwainodaichi and UNICULM. It was also demonstrated that the senescence in the flag leaves, which was indicated by the decline of the photosynthetic rate, was accelerated by the waterlogging from the jointing stage till maturity (Fig. 4). The accelerated senescence under waterlogging is similar to abnormal early ripening that occurs in waterlogging-prone area (Hossain et al., 2011). Araki et al. (2012) also suggested that root injury by waterlogging at jointing induces rapid leaf senescence in the grain filling period, although they did not show any data on the root growth under waterlogging. Next, we found that the relative root length density was decreased greater in UNICULM, followed by Iwainodaichi and Nishikazekomugi under waterlogged conditions in comparison to control (Table 3). Because root length is an important factor that determines the size of contact with soil and thus the capability of water and nutrient uptake (Gowda et al., 2011), this result indicates that the greater root development under waterlogging is related to the waterlogging tolerance in Nishikazekomugi and Iwainodaichi. This is consistent with the results that leaf water potential was maintained higher in Nishikazekomugi and Iwainodaichi under waterlogging than in UNICULM. These indicate that the greater root development under waterlogging is involved in higher leaf water potential, and consequently stomatal conductance, photosynthetic rate and higher grain yield in wheat. Further study will need to be performed to determine the relationship between greater root development and higher stomatal conductance and photosynthetic rate in waterlogging-tolerant wheat cultivars by using near-isogenic lines with higher maintenance of root development under waterlogging.
The mechanism on how root development was maintained under waterlogging in Nishikazekomugi and Iwainodaichi remains unclear. When plants suffer by waterlogging, the roots become O2 deficient and growth finally stops (Jackson and Armstrong, 1999; Malik et al., 2003). Therefore, the formation of aerenchyma in roots is one of the important traits for maintaining root growth under waterlogging by supplying O2 to the root apex (Armstrong, 1971; Arikado, 1975; Colmer, 2003; Setter and Waters, 2003). We anticipated that waterlogging-tolerant cultivars may have an advantage for the formation of aerenchyma in the roots under waterlogging, which promotes root development. It was also reported that the enhanced lateral root formation contributes to maintaining high root length density and consequently to high drought tolerance in rice under water supply-limited conditions (Kano et al., 2011). We need to investigate how and which root traits such as aerenchyma formation and lateral root development are necessary for the maintained root length density in the waterlogging-tolerant wheat cultivars in further study. In addition, the water absorption ability in plants is defined by not only the root length but also the hydraulic conductance of roots. In this study, we showed that the maintained root length density is correlated with the waterlogging tolerance in wheat, although root hydraulic conductance was not determined. In a future study, it is needed to elucidate whether the hydraulic conductance in roots is also an important factor for waterlogging tolerance in wheat. In conclusion, we have found that the maintained root development is an important quantitative trait to maintain water uptake under waterlogged conditions, and is positively correlated with the leaf water potential, stomatal conductance and photosynthetic rate in the flag leaf of waterlogging-tolerant wheat cultivars. Therefore,
Please cite this article in press as: Hayashi, T., et al., Maintained root length density contributes to the waterlogging tolerance in common wheat (Triticum aestivum L.). Field Crops Res. (2013), http://dx.doi.org/10.1016/j.fcr.2013.03.020
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Fig. 5. Photosynthetic rate of Nishikazekomugi, Iwainodaichi and UNICULM under control () and waterlogged (䊉) conditions in 2008–2010. Data are means of 5 replicates. ** indicates significant difference between the control and waterlogged conditions at each period (P < 0.01).
Fig. 6. Relationship between root length density and stomatal conductance of Nishikazekomugi (), Iwainodaichi ( ) and UNICULM (䊉) under control and waterlogged conditions in 2008–2010. The data on stomatal conductance at 15, 17 and 16 d after the start of waterlogging in 2008–2010, respectively (Fig. 4), were used for correlation analysis. Control, r = 0.67**; waterlogging, r = 0.83**; **P < 0.01.
greater root development is suggested to be involved in improving the grain yield in wheat plants under waterlogged conditions. It is interesting to note that the maintained root development is also a key trait for the adaptation in rice under progressive drought (Kano et al., 2011), drought to rewatering (Siopongco et al., 2005), transient waterlogging to drought and vice versa (Suralta et al., 2008a,b, 2010; Suralta and Yamauchi, 2008) and continuous cycle of alternate waterlogging to drought (Niones et al., 2012, 2013). Roots also produce signals in response to progressive drought, which regulates stomatal conductance, transpiration and shoot growth (Siopongco et al., 2008). These suggest that root development
plasticity is essential to tolerate water-limited environment caused by drought or waterlogging-induced root injury. The waterloggingtolerant wheat cultivars found in this study will be available to elucidate the quantitative mechanism of the plastic development of roots under waterlogging tolerance in wheat. Acknowledgements The authors would like to thank Ms. Violeta Bartolome of International Rice Research Institute for assistance in statistical analysis and Dr. Joyce A. Cartagena of Nagoya University for editing and
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Please cite this article in press as: Hayashi, T., et al., Maintained root length density contributes to the waterlogging tolerance in common wheat (Triticum aestivum L.). Field Crops Res. (2013), http://dx.doi.org/10.1016/j.fcr.2013.03.020