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Field Crops Research 165 (2014) 36–48 Contents lists available at ScienceDirect Field Crops Research journal homepage: www.elsevier.com/locate/fcr Reprint of “Morphological and physiological traits of roots and their relationships with water productivity in water-saving and drought-resistant rice” Guang Chu a , Tingting Chen a , Zhiqin Wang a , Jianchang Yang a,, Jianhua Zhang b,1 a Key Laboratory of Crop Genetics and Physiology of Jiangsu Province, Yangzhou University, Yangzhou, Jiangsu, China b School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Hong Kong, China article info Article history: Received 7 September 2013 Received in revised form 5 November 2013 Accepted 12 November 2013 Available online 17 July 2014 Keywords: Water-saving and drought-resistant rice (Oryza sativa L.) Root morpho-physiological traits Grain filling Alternate wetting and drying Grain yield Water productivity. abstract Water-saving and drought-resistant rice (WDR) could substantially reduce irrigation water and mean- while produce higher grain yield compared with paddy rice under water-saving irrigation. The mechanism underlain, however, is yet to be understood. We investigated if improved root traits would contribute to an increase in water productivity in WDR. Two rice varieties, each for WDR and paddy rice, were field-grown with two irrigation methods, continuous flooding (CF) and alternate wetting and drying (AWD) irrigation, which were imposed during the whole growing season. Under CF, grain yield, water productivity (grain yield over amount irrigation water and precipitation) and root morpho-physiological traits, such as root biomass and root oxidation activity (ROA), showed no significant difference between WDR and paddy rice. Under AWD, however, WDR exhibited greater root dry weight, root length density, ROA, total absorbing surface area and active absorbing surface area of roots, greater zeatin (Z) + zeatin riboside (ZR) contents in both roots and leaves, and higher activities of enzymes involved in sucrose- to-starch conversion in grains during grain filing, in relative to paddy rice. Grain yield under AWD was significantly decreased for paddy rice compared with that under CF, but showed no significant difference for WDR between the two irrigation treatments. The WDR variety increased grain yield by 9.2–13.4% and water productivity by 9.0–13.7% over the paddy rice variety under AWD. The root dry weight was signif- icantly correlated with shoot dry weight, and ROA and root Z + ZR content were significantly correlated with leaf photosynthetic rate, Z + ZR content in leaves and activities of key enzymes involved in sucrose- to-starch conversion in grains. Collectively, the data suggest that improved morpho-physiological traits, as showing a greater root biomass, root length density, ROA and root Z + ZR content, contributes to higher grain yield and water productivity for WDR under water-saving irrigation. © 2014 Elsevier B.V. All rights reserved. 1. Introduction Rice (Oryza sativa L.) is one of the most important food crops in the world and consumed by more than 3 billion people (Fageria, DOI of original article: http://dx.doi.org/10.1016/j.fcr.2013.11.006. Abbreviations: AGPase, adenosine diphosphoglucose pyrophosphorylase; AWD, alternate wetting and drying; CF, continuous flooding; DAT, days after transplan- ting; DW, dry weight; ROA, root oxidation activity; StSase, starch synthase; SuSase, sucrose synthase; WDR, water-saving and drought-resistant rice; Z, zeatin; ZR, zeatin riboside. This article is a reprint of a previously published article. For citation purposes, please use the original publication details “Field Crops Research” 162 (2014) 108–119. Corresponding author. Tel.: +86 514 8797 9317, fax: +86 514 8797 9317. E-mail addresses: [email protected], [email protected] (J. Yang), [email protected] (J. Zhang). 1 Tel.: +852 3943 6288, fax: +852 2603 6382. 2007). It is estimated that, by the year 2025, it will be necessary to produce about 60% more rice than what is currently produced to meet the food needs of a growing world population (Fageria, 2007). Rice is also the greatest consumer of water among all crops and consumes about 80% of the total irrigated fresh water resources in Asia (Bouman and Tuong, 2001). Fresh water, however, is becom- ing increasingly scarce because of population growth, increasing urban and industrial development, and the decreasing availability resulting from pollution and resource depletion (Belder et al., 2004; Bouman, 2007). To meet the major challenge that rice production needs to increase to feed a growing population under increasing scarcity of water resources, water-saving and drought-resistant rice (WDR) varieties have been bred (Luo, 2010) and alternate wetting and drying (AWD) irrigation has been developed as a novel water-saving technique (Bouman and Tuong, 2001; Yang et al., 2007; Yao et al., 2012; Zhang et al., 2009). http://dx.doi.org/10.1016/j.fcr.2014.06.026 0378-4290/© 2014 Elsevier B.V. All rights reserved.

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Page 1: Reprint of “Morphological and physiological traits of roots and their relationships with water productivity in water-saving and drought-resistant rice”

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Field Crops Research 165 (2014) 36–48

Contents lists available at ScienceDirect

Field Crops Research

journa l homepage: www.e lsev ier .com/ locate / fc r

eprint of “Morphological and physiological traits of roots and theirelationships with water productivity in water-saving androught-resistant rice”�

uang Chua, Tingting Chena, Zhiqin Wanga, Jianchang Yanga,∗, Jianhua Zhangb,1

Key Laboratory of Crop Genetics and Physiology of Jiangsu Province, Yangzhou University, Yangzhou, Jiangsu, ChinaSchool of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Hong Kong, China

r t i c l e i n f o

rticle history:eceived 7 September 2013eceived in revised form 5 November 2013ccepted 12 November 2013vailable online 17 July 2014

eywords:ater-saving and drought-resistant rice

Oryza sativa L.)oot morpho-physiological traitsrain fillinglternate wetting and dryingrain yieldater productivity.

a b s t r a c t

Water-saving and drought-resistant rice (WDR) could substantially reduce irrigation water and mean-while produce higher grain yield compared with paddy rice under water-saving irrigation. Themechanism underlain, however, is yet to be understood. We investigated if improved root traits wouldcontribute to an increase in water productivity in WDR. Two rice varieties, each for WDR and paddy rice,were field-grown with two irrigation methods, continuous flooding (CF) and alternate wetting and drying(AWD) irrigation, which were imposed during the whole growing season. Under CF, grain yield, waterproductivity (grain yield over amount irrigation water and precipitation) and root morpho-physiologicaltraits, such as root biomass and root oxidation activity (ROA), showed no significant difference betweenWDR and paddy rice. Under AWD, however, WDR exhibited greater root dry weight, root length density,ROA, total absorbing surface area and active absorbing surface area of roots, greater zeatin (Z) + zeatinriboside (ZR) contents in both roots and leaves, and higher activities of enzymes involved in sucrose-to-starch conversion in grains during grain filing, in relative to paddy rice. Grain yield under AWD wassignificantly decreased for paddy rice compared with that under CF, but showed no significant differencefor WDR between the two irrigation treatments. The WDR variety increased grain yield by 9.2–13.4% andwater productivity by 9.0–13.7% over the paddy rice variety under AWD. The root dry weight was signif-

icantly correlated with shoot dry weight, and ROA and root Z + ZR content were significantly correlatedwith leaf photosynthetic rate, Z + ZR content in leaves and activities of key enzymes involved in sucrose-to-starch conversion in grains. Collectively, the data suggest that improved morpho-physiological traits,as showing a greater root biomass, root length density, ROA and root Z + ZR content, contributes to highergrain yield and water productivity for WDR under water-saving irrigation.

© 2014 Elsevier B.V. All rights reserved.

. Introduction

Rice (Oryza sativa L.) is one of the most important food crops inhe world and consumed by more than 3 billion people (Fageria,

DOI of original article: http://dx.doi.org/10.1016/j.fcr.2013.11.006.Abbreviations: AGPase, adenosine diphosphoglucose pyrophosphorylase; AWD,

lternate wetting and drying; CF, continuous flooding; DAT, days after transplan-ing; DW, dry weight; ROA, root oxidation activity; StSase, starch synthase; SuSase,ucrose synthase; WDR, water-saving and drought-resistant rice; Z, zeatin; ZR,eatin riboside.� This article is a reprint of a previously published article. For citation purposes,lease use the original publication details “Field Crops Research” 162 (2014) 108–119.∗ Corresponding author. Tel.: +86 514 8797 9317, fax: +86 514 8797 9317.

E-mail addresses: [email protected], [email protected] (J. Yang),[email protected] (J. Zhang).

1 Tel.: +852 3943 6288, fax: +852 2603 6382.

ttp://dx.doi.org/10.1016/j.fcr.2014.06.026378-4290/© 2014 Elsevier B.V. All rights reserved.

2007). It is estimated that, by the year 2025, it will be necessary toproduce about 60% more rice than what is currently produced tomeet the food needs of a growing world population (Fageria, 2007).Rice is also the greatest consumer of water among all crops andconsumes about 80% of the total irrigated fresh water resources inAsia (Bouman and Tuong, 2001). Fresh water, however, is becom-ing increasingly scarce because of population growth, increasingurban and industrial development, and the decreasing availabilityresulting from pollution and resource depletion (Belder et al., 2004;Bouman, 2007). To meet the major challenge that rice productionneeds to increase to feed a growing population under increasingscarcity of water resources, water-saving and drought-resistant

rice (WDR) varieties have been bred (Luo, 2010) and alternatewetting and drying (AWD) irrigation has been developed as a novelwater-saving technique (Bouman and Tuong, 2001; Yang et al.,2007; Yao et al., 2012; Zhang et al., 2009).
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s Research 165 (2014) 36–48 37

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Table 1Precipitation, sunshine hours, and mean temperature during the growing season ofrice in 2011 and 2012 in Yangzhou, Southeast China.

May June July August September October

Precipitation (mm per month)2011 103 195 309 232 48.2 38.62012 38.2 32.2 195 213 60.6 27.2

Sunshine (h per month)2011 241 118 143 115 159 1632012 202 101 173 122 172 171

Mean temperature (◦C)2011 21.9 24.4 27.5 26.7 22.7 20.42012 22.1 25.3 29.3 27.9 22.2 19.5

G. Chu et al. / Field Crop

WDR is a new type of rice variety which has high yield potentialnd good quality as the current paddy rice, as well as the capacityf water-saving or drought resistance (Luo, 2010; Luo et al., 2011).here are reports showing that WDR could reduce water consump-ion by about 50% meanwhile could not markedly decease grainield compared with paddy rice (Luo, 2010; Luo et al., 2011; Zhangt al., 2012a), although there is an observation that the super hybridice variety Yangliangyou 6 produced 21.5% higher grain yield thanhe WDR variety Hanyou 3 under AWD conditions (Yao et al., 2012).he mechanism that WDR has high yield potential and capacity ofater-saving has yet to be understood.

In AWD, irrigation is applied a few days after water has dis-ppeared from the surface so that periods of soil submergencelternate with periods of non-submergence during the whole grow-ng season (Belder et al., 2004; Tuong et al., 2005; Yao et al.,012). This technique could substantially reduce irrigation waternd maintain or even increase grain yield because of the enhance-ent in nutrient uptake by rice plants, root growth, grain filling

ate, and remobilization of carbon reserves from vegetative tissueso grains, in relative to continuous flooding (CF) irrigation (Beldert al., 2004; Liu et al., 2013; Tuong et al., 2005; Yao et al., 2012;hang et al., 2008, 2009, 2012b). Although the AWD technology haseen researched extensively in countries such as China, India, andhilippines, the physiological mechanism involved in the effect ofWD on the yield and water productivity remains to be elucidated.

As an integral part of plant organs, roots are involved in acqui-ition of nutrients and water, synthesis of plant hormones, organiccids and amino acids, and anchorage of plants (Yang et al.,004a,b). Root morphology and physiology are closely associatedith the growth and development of aboveground plants (Osaki

t al., 1997; Samejima et al., 2004; Yang et al., 2008; Zhang et al.,009). However, information on root morphology and physiologynd their relationship with grain yield and water productivity inDR is unavalable.The objectives of this study were to (1) investigate the yield

erformance of WDR under both CF and AWD conditions, (2) makeomparison between WDR and paddy rice in root morphologicalnd physiological traits, and (3) analyze the relationship betweenoot morpho-physiological traits and shoot growth and activity.oot biomass, root oxidation activity (ROA), root length density,oot diameter, root total absorbing surface area, root active absorb-ng surface area and zeatin (Z) + zeatin riboside (ZR) contents inoots were defined as root morphological and physiological traitsSamejima et al., 2005; Yang et al., 2012; Zhang et al., 2009). Shootiomass, leaf photosynthetic rate, Z + ZR content in leaves, andctivities of some key enzymes involved in sucrose-to-starch con-ersion in grains, sucrose synthase (SuSase, EC 2.4.1.13), adenosineiphosphoglucose pyrophosphorylase (AGPase, EC 2.7.7.27), andtarch synthase (StSase, EC 2.4.1.21), were used as indices of shootrowth and activity. The hypothesis is that improved root traits canenefit shoot growth, and consequently, contribute to an increase

n water productivity in WDR under water-saving irrigation.

. Materials and methods

.1. Plant materials and growth conditions

Field experiments were conducted at a research farm ofangzhou University, Jiangsu Province, China (32o30′N, 119o25′E,1 m altitude) during the rice growing season (May–October) in011, and repeated in 2012. The soil was a sandy loam (Typic

uvaquents, Etisols, US classification) that contained 24.2 g kg−1

rganic matter, 103 mg kg−1 alkali hydrolysable N, 34.5 mg kg−1

lsen-P and 68.6 mg kg−1 exchangeable K in 0–20 cm soil depth.he field capacity soil moisture content, measured after constant

Precipitation and sunshine hours are monthly totals. Temperatures are the monthlyaverages.

drainage rate and made gravimetrically, was 0.188 g g−1, and bulkdensity of the soil was 1.33 g cm−3. The average air temperature,precipitation, and sunshine hours during the rice growing seasonacross the two study years measured at a weather station close tothe experimental site are shown in Table 1.

A WDR (Oryza sativa L.) variety Hanyou 8 (HY8, a japonica hybridfrom the cross Huhan 2A × Huhan 2B) and a high-yielding paddyrice variety Lingxiangyou 18 (LXY18, a japonica hybrid from thecross Lingxiang A × YC418) were grown in the field. Both vari-eties are currently planted in local production. Except for droughtresistance, both varieties have similar traits with plant height105–110 cm, the whole growth period 152–155 days, 17 leaves inthe main stem, thick culms and erect upper leaves, and are suit-able for planting in the lower reaches of Yangtze River of China(Li et al., 2009; Yu et al., 2011). Seeds of HY8 were provided byShanghai Agrobiological Gene Center (Shanghai, China) and thoseof LXY18 were obtained from College of Agriculture, Yangzhou Uni-versity (Yangzhou, China). Seedlings were raised in the field withsowing date on 15 May and transplanted on 10 June at a hill spac-ing of 25 cm × 16 cm with two seedlings per hill. N (60 kg ha−1 asurea, P (45 kg ha−1 as single superphosphate) and K (60 kg ha−1

as KCl) were applied and incorporated before transplanting. N asurea was also applied at mid-tillering (40 kg ha−1), panicle ini-tiation (25 kg ha−1) and at the initial of spikelet differentiation(25 kg ha−1). Both varieties (50% of plants) headed on 25–26 August,and were harvested on 15–16 October.

2.2. Treatments

The experiment was laid out in a complete randomized blockdesign with three replicates. Plot dimension was 8 m × 4.8 m andplots were separated by a 1-m wide alley using plastic film insertedinto the soil to a depth of 50 cm. Two irrigation regimes (treat-ments), alternate wetting and soil drying (AWD) and continuousflooding (CF), were conducted from 10 days after transplanting(DAT), at which seedlings were recovered from transplantinginjury, to maturity. In AWD, plants were not re-watered untilthe soil water potential reached −15 kPa (soil moisture content0.172 g g−1) at 15–20 cm depth. Except drainage at the mid-season,the CF regime was continuously flooded with 2–3 cm water level inthe plot until one week before harvest in line with traditional farm-ing practice. Soil water potential in the AWD plot was monitoredat 15–20-cm soil depth with a tensionmeter consisting of a sen-sor of 5 cm length. Four tensionmeters were installed in each plot,

and readings were recorded at 12:00 h each day. When the read-ing reached the threshold, a flood with 2–3 cm water depth wasapplied to the plots. The amount of irrigation water was monitoredwith a flow meter (LXSG-50 Flow meter, Shanghai Water Meter
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anufacturing Factory, Shanghai, China) installed in the irrigationipelines.

.3. Sampling and measurements

Leaf water potentials of the top full-expanded leaves were deter-ined at midday (11:30 h) at 41, 52, 66, 90, and 101 DAT in 2011

nd at 40, 51, 74, 91 and 102 DAT in 2012 when days were clearnd soil water potential was approximately −15 kPa in the AWDegime. A pressure chamber (Model 3000, Soil Moisture Equipmentorp., Santa Barbara, CA, USA) was used for leaf water potentialeasurement, with six leaves for each treatment.Root and shoot biomass, root length, root length density, spe-

ific root length, root diameter, root total absorbing surface areand root active absorbing surface area were determined at 19–20,0–41, 75–76 and 124–125 DAT. The growth stages correspond-

ng above dates were mid-tillering, panicle initiation, heading timend maturity, respectively. ROA, Z + ZR contents in both roots andeaves, leaf photosynthetic rate, and activities of SuSase, AGPasend StSase in grains were determined at 90–91 (D1) and 101–102D2) DAT when soil water potential was about −15 kPa in the AWDlot and at 92–93 (W1) and 103–104 (W2) DAT when plants wereewatered. To maintain canopy conditions, the vacant spaces leftfter sampling for measurements of root and shoot biomasses weremmediately replaced with hills taken from the borders and theseeplanted hills were not subjected to sampling any more.

For each root sampling, a cube of soil (25 cm in length × 16 cm inidth × 20 cm in depth) around each individual hill was removedp using a sampling core. Such a cube contains approximately 95%f total root biomass (Kukal and Aggarwal, 2003; Yang et al., 2008).

lants of five hills from each plot formed a sample at each mea-urement. The cube of soil was cut into two parts, with 10 cmepth for each part. The roots in each cube of soil were carefullyinsed with hydropneumatic elutriation device (Gillison’s Variety

ig. 1. Soil water potentials for the water-saving and drought-resistant rice variety HY8nd alternate wetting and drying (AWD) irrigation in 2011 (A and C) and 2012 (B and D)ars represent ± standard error of the mean (n = 12) where these exceed the size of the sy

arch 165 (2014) 36–48

Fabrications, Benzonia, MI, USA). After combining roots of five hillsand recording fresh weight, about 10 g roots from each sample werefrozen in liquid N for 1 min and then stored at −80 ◦C for hormonalassay. Portions of each root sample were used for measurementsof root length, root diameter, and ROA. The rest of the roots weredried in an oven at 70 ◦C to constant weight and weighed. To mea-sure root length and diameter, roots were arranged and floatedon shallow water in a glass tray (30 cm × 30 cm) and then scannedusing a scanner (Epson Expression 1680 Scanner, Seiko Epson Corp.,Tokyo, Japan) and analyzed using WinRHIZO Root Analyzer System(Regent Instruments Inc., Quebec, Canada). Root length density wascalculated from the root length and the volume of the soil core(V), i.e. root length density (cm cm−3) = root length (cm)/V (cm3).Specific root length was calculated from the root length and rootdry weight (DW), that is, specific root length (m g−1 DW) = rootlength (m)/root dry weight (g). Root total absorption area and activeabsorption area of fresh root samples were determined by methy-lene blue dyeing method (Zhang, 1998). The ROA was determinedby measuring oxidation of alpha-naphthylamine (�-NA) accordingto the method of Ramasamy et al. (1997), and was expressed as�g �-NA per gram DW per hour (�g �-NA g−1 DW h−1). Before rootsampling, aboveground plants were sampled and separated intoleaves, stems, panicles (from heading) and dead shoot parts, andwere dried in an oven at 70 ◦C to constant weight for determiningshoot biomass.

The photosynthetic rate of the flag leaf was measured with agas exchange analyze (Li-Cor 6400 portable photosynthesis mea-surement system, Li-Cor, Lincoin, NE, USA). The measurement wasmade during 09:00–11:00 h when photosynthetic active radiationabove the canopy was 1300–1400 �mol m−2 s−1. Nine leaves were

used for each treatment. Six flag leaves from each treatment at eachmeasurement date (D1, D2, W1, W2) were sampled and frozen inliquid N for 1 min and then stored at −80 ◦C for determining Z andZR content.

(A and B) and paddy rice variety LXY18 (C and D) under continuous flooding (CF). Arrows in the figures indicate mid-season drainage for the CF treatment. Verticalmbol.

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s Research 165 (2014) 36–48 39

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Fig. 2. Leaf water potentials of the water-saving and drought-resistant rice varietyHY8 and paddy rice variety LXY18 under continuous flooding (CF) and alternatewetting and drying (AWD) irrigation in 2011 (A) and 2012 (B). Measurements were

G. Chu et al. / Field Crop

The methods for extraction and purification of Z and ZR in rootsnd leaves were as described by Bollmark et al. (1988) and He1993). The quantification of Z and ZR was analyzed by an enzyme-inked immunosorbent assay (ELISA) and was described previouslyYang et al., 2001, 2002). The contents of Z + ZR in roots or leavesere expressed as pmol or nmol g−1 DW. Recoveries of Z and ZRere 78.3–80.7% in roots and 75.6–78.5% in leaves. Activities of

uSase, AGPase and StSase in grains were determined according tohe method described by Yang et al. (2003, 2004a,b). Activities ofnzymes were expressed as nmol mg−1 protein min−1. Protein con-ent was determined according to Bradford (1976), using bovineerum albumin as standard.

Plants were hand-harvested on 15 October in 2011 and 16ctober in 2012. The measurement of grain yield and yield com-onents was followed the procedure as described by Yoshida et al.1976). Plants in two rows on each side of the plot were discardedo avoid border effects. Grain yield was determined from a harvestrea of 6.0 m2 in each plot and adjusted to 14% moisture. Above-round biomass and yield components, i.e. the number of panicleser square meter, number of spikelets per panicle, percentage oflled grains, and grain weight, were determined from plants of.6 m2 (excluding the border ones) sampled randomly from eachlot. The percentage of filled grains was defined as the filled grainsspecific gravity ≥ 1.06 g cm−3) as a percentage of total number ofpikelets.

.4. Statistical analysis

Analysis of variance was performed using SAS/STAT statis-ical analysis package (version 6.12, SAS Institute, Cary, NC,SA). The statistical model used included sources of vari-tion due to replication, year, variety, irrigation treatment,nd the interaction of year × variety, year × treatment and vari-ty × treatment. Data from each sampling date were analyzedeparately. Means were tested by least significant difference at P =.05 (LSD0.05).

. Results

.1. Soil and leaf water potentials

The differences in sunshine hours and mean temperature wereather small between 2011 and 2012 (Table 1). Although the totalainfall from transplanting to maturity was more in 2011 (802 mm)han in 2012 (528 mm), the rainfall during the mid and late growingeason (from August through October) showed no much differenceetween the two years (319 mm in 2011 and 301 mm in 2012).hanges in soil water potentials in the AWD plot were similar inoth years for both WDR and paddy rice varieties (Fig. 1A–D). Itook 6–10 days to reach soil water potential of −15 kPa dependingn plant growth stages.

Fig. 2 shows the changes in mid-day (11:30 h) leaf water poten-ials under both CF and AWD treatments and when soil waterotentials were approximately −15 kPa in the AWD plot. For plantsrown under CF conditions, mid-day leaf water potential rangedrom approximately −0.57 megapascal (MPa) at 40 or 41 DATo about −0.98 MPa at 101 or 102 DAT, and showed no signifi-ant difference between WDR and paddy rice. Leaf water potentialas reduced under AWD conditions, and ranged from −0.84 to

1.47 MPa, with much more reduction for the paddy rice varietyXY18 than for the WDR variety HY8 (Fig. 2A and B), indicatinghat WDR could maintain a higher water status than paddy ricehen plants subjected to soil-drying.

made on the upmost fully expanded leaves at midday (11:30 h) when soil waterpotential was about −15 kPa under AWD. Vertical bars represent ± standard errorof the mean (n = 6) where these exceed the size of the symbol.

3.2. Root traits and shoot biomass

Root and shoot biomass and root/shoot ratios at different growthstages are presented in Fig. 3. Root DW of the WDR variety HY8showed no significant difference between CF and AWD treatmentsat all the measurement stages. However, the AWD treatment signif-icantly decreased root DW of the paddy rice variety LXY18 whencompared with the CF. Under the CF treatment, the difference inroot DW was not significantly different between HY8 and LXY18(Fig. 3C and D). A very similar observation was made on shoot DW(Fig. 3A and B). Although the root/shoot ratio was a little higherunder AWD than under CF, it showed no significant differencebetween the two irrigation regimes or between the two kinds ofvarieties at each measurement date (Fig. 3E and F). Regression anal-ysis showed that shoot DW significantly correlated with root DW(r = 0.89**, P = 0.01, n = 16), implying that shoot dry matter produc-tion interacts with root biomass.

Further observation showed that root biomass in 0–10 cm soildepth was greater under CF than under AWD, but the result wasreversed for root biomass in 11–20 cm soil depth for both vari-eties (Table 2). When comparison was made between HY8 andLXY18, there was no significance in root biomass in 0–10 cm soildepth under CF, whereas HY8 had greater root biomass than LXY18

under AWD, especially in 11–20 cm soil depth. For example, rootdry weight (t ha−1) in 11–20 cm soil depth at panicle initiation,heading time, and maturity was 0.32, 0.42, and 0.27, respectively,for HY8, whereas it was 0.24, 0.34, and 0.20, respectively, for LXY18
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40 G. Chu et al. / Field Crops Research 165 (2014) 36–48

Fig. 3. Shoot dry weight (A and B), root dry weight (C and D) and root/shoot ratio (E and F) of the water-saving and drought-resistant rice variety HY8 and paddy rice varietyLXY18 under continuous flooding (CF) and alternate wetting and drying (AWD) irrigation in 2011 (A, C and E) and 2012 (B, D and F). MT, PI, HT and Mu represent mid-tillering,p stanl the sa

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anicle initiation, heading time and maturity, respectively. Vertical bars represent ±etters above the column indicate statistical significance at the P = 0.05 level within

Table 2), indicating a deeper root distribution in soil for WDR thanor paddy rice.

.3. Root length, diameter and absorption area

Root length, root length density and specific root lengthxhibited a similar changing pattern during the growing season

Fig. 4A–F). They showed no significant difference between HY8nd LXY18 under CF, but root length and root length density wereignificantly greater for the former than for the latter under AWD.

hen compared with CF, AWD significantly reduced root length,

dard error of the mean (n = 6) where these exceed the size of the symbol. Differentme measurement stage, and NS means not significant at the P = 0.05 level.

root length density and specific root length of LXY8 throughout thegrowing season and those of HY8 at heading time and maturity.

Except at maturity at which root diameter was greater underAWD than under CF, difference in root diameter was not signifi-cant between CF and AWD or between HY8 and LXY18 at othergrowth stages (Fig. 4G and F), implying that greater root biomass,root length density and specific root length for WDR than forpaddy rice under AWD are mainly attributed to larger number of

roots.

Similar to root biomass, the total absorption area of roots underAWD were markedly decreased for LXY18 compared with thoseunder CF, whereas it showed no significant difference between

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G. Chu et al. / Field Crops Research 165 (2014) 36–48 41

Fig. 4. Root length (A and B), root length density (C and D), specific root length (E and F) and root diameter (G and H) of the water-saving and drought-resistant rice varietyHY8 and paddy rice variety LXY18 under continuous flooding (CF) and alternate wetting and drying (AWD) irrigation in 2011 (A, C, E, and G) and 2012 (B, D, F and H). MT,PI, HT and Mu represent mid-tillering, panicle initiation, heading time and maturity, respectively. Vertical bars represent ± standard error of the mean (n = 3) where theseexceed the size of the symbol. Different letters above the column indicate statistical significance at the P = 0.05 level within the same measurement stage, and NS means notsignificant at the P = 0.05 level.

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42 G. Chu et al. / Field Crops Research 165 (2014) 36–48

Table 2Root dry weight (t ha−1) in the 0–10 cm and 11–20 cm soil layer for the water-saving and drought-resistant rice variety HY8 and paddy rice variety LXY18 under continuousflooding (CF) and alternate wetting and drying (AWD) irrigation.a

Year/variety Irrigation Panicle initiation Heading time Maturity

0–10 cm 11–20 cm 0–10 cm 11–20 cm 0–10 cm 11–20 cm

2011HY8 CF 1.03a 0.23b 1.13a 0.32cd 1.18ab 0.19bc

AWD 0.92b 0.31a 1.04b 0.41a 1.10c 0.26a

LXY18 CF 1.04a 0.21c 1.16a 0.31d 1.22a 0.18cAWD 0.81c 0.23b 0.98c 0.33bc 1.03de 0.20b

2012HY8 CF 1.00a 0.24b 1.16a 0.31d 1.16b 0.19bc

AWD 0.91b 0.32a 1.04b 0.42a 1.06 cd 0.27a

LXY18 CF 1.03a 0.23b 1.15a 0.32 cd 1.20ab 0.19bcAWD 0.82c 0.24b 0.96c 0.34b 0.99e 0.20b

Analysis of varianceYear (Yr) NSa NS NS NS NS NSVariety (V) NS 5.7* NS 6.9* NS 4.8*

Treatment (T) 25.4** 16.8** 18.7** 12.5** 13.3** 10.2**

Yr × V NS NS NS NS NS NSYr × T NS NS NS NS NS NSV × T NS NS NS NS NS NS

a NS, Not significant at the P = 0.05 level.* Significant at the P = 0.05 level.

** Significant at the P = 0.01 level.

Fig. 5. Total absorption area (A and B), and active absorption area (C and D) of roots of the water-saving and drought-resistant rice variety HY8 and paddy rice variety LXY18under continuous flooding (CF) and alternate wetting and drying (AWD) irrigation in 2011 (A and C) and 2012 (B and D). MT, PI, HT and Mu represent mid-tillering, panicleinitiation, heading time and maturity, respectively. Vertical bars represent ± standard error of the mean (n = 3) where these exceed the size of the symbol. Different lettersabove the column indicate statistical significance at the P = 0.05 level within the same measurement stage, and NS means not significant at the P = 0.05 level.

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G. Chu et al. / Field Crops Research 165 (2014) 36–48 43

Fig. 6. Root oxidation activity (A and B) and zeatin (Z) + zeatin riboside (ZR) content in roots (C and D) of the water-saving and drought-resistant rice variety HY8 and paddyrice variety LXY18 under continuous flooding (CF) and alternate wetting and drying (AWD) irrigation in 2011 (A and C) and 2012 (B and D). D1 and D2 are measurement timeat 90–91 and 101–102 days after transplanting when soil water potential was about −15 kPa in the AWD plot, and W1 and W2 are measurement time at 92–93 and 103–104d darda e me

tsWap

3

wudpA(pWnsa

(admwnf

ays after transplanting when plants were re-watered. Vertical bars represent ± stanbove the column indicate statistical significance at the P = 0.05 level within the sam

he two irrigation regimes for HY18 (Fig. 5A and B). The AWDignificantly decreased the active absorption area of roots for both

DR and paddy rice, with more decrease for paddy rice (Fig. 5Cnd D), indicating that WDR could keep higher root activity thanaddy rice under water-saving irrigation.

.4. ROA and Z + ZR contents in roots and leaves

To understand whether physiological performance of rootsould be different between at soil-drying and at wetting timender AWD, ROA and Z + ZR content in roots were measureduring the soil-drying period and the re-watering time. When com-ared with those under CF, ROA and root Z + ZR contents underWD were significantly decreased during the soil-drying period

D1 and D1) for both kinds of varieties, with more decrease foraddy rice (Fig. 6A–D). During the re-watering time (W1 and2), however, both ROA and root Z + ZR contents were pro-

ouncedly increased for the WDR variety HY8, and showed noignificant differences for the paddy rice variety LXY18 between CFnd AWD.

Similar results were observed for Z + ZR contents in leavesFig. 7A and B) and the photosynthetic rate of the flag leaf (Fig. 7Cnd D). Both leaf Z + ZR content and photosynthetic rate wereecreased during the soil-drying period for both varieties, with

ore decrease for LXY18 than for HY8. At the re-watering time, theyere significantly higher under AWD than CF for HY8, and showedo significant differences between the two irrigation treatments

or LXY18.

error of the mean (n = 3) where these exceed the size of the symbol. Different lettersasurement date.

3.5. Activities of enzymes in grains

Activities of the three enzymes involved in sucrose-to-starchconversion in grains, SuSase, AGPase and StSase, are presented inFig. 8. For the WDR variety HY8, activities of the three enzymesunder AWD were not markedly decreased during the soil-dryingperiod, but they were significantly increased at the re-wateringtime compared with those under CF. In contrast to those of HY8, theenzymatic activities in grains for the paddy rice LXY18 under AWDwere significantly decreased at the soil-drying time, although theirdifferences were not significant between CF and AWD during there-watering period (Fig. 8A–F). The results suggest that there are re-watering effects on root and shoot physiology, and indicate againthat WDR possesses higher root and shoot activities than paddyrice when subjected to soil-drying.

Regression analysis showed that ROA and root Z + ZR contentsignificantly correlated with leaf Z + ZR content, photosynthetic rateof the flag leaf and activities of the three enzymes in grains duringgrain filling (Table 3). The result indicates again that shoot growthis closely associated with root growth.

3.6. Grain yield and water productivity

When compared with that under CF, grain yield under AWD

was significantly lower for LXY18, but showed no significantdifference for HY8 (Table 4). In comparison between the two kindsof varieties, WDR showed significant higher grain yield than paddyrice under AWD, with an increase rate by 9.2–13.4%, although
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44 G. Chu et al. / Field Crops Research 165 (2014) 36–48

Fig. 7. Zeatin (Z) + zeatin riboside (ZR) content in leaves (A and B) and photosynthetic rate of the flag leaf (C and D) of the water-saving and drought-resistant rice varietyHY8 and paddy rice variety LXY18 under continuous flooding (CF) and alternate wetting and drying (AWD) irrigation in 2011 (A and C) and 2012 (B and D). D1 and D2are measurement time at 90–91 and 101–102 days after transplanting when soil water potential was about −15 kPa in the AWD plot, and W1 and W2 are measurementt Verticl rs abom

nTrAvac

2(tobw22

yield, leading to greater water productivity in WDR (Figs. 3 and 9;

TCa

ime at 92–93 and 103–104 days after transplanting when plants were re-watered.eaf photosynthetic rate) where these exceed the size of the symbol. Different lette

easurement date.

o significant difference in grain yield was observed under CF.he number of panicles and spikelets per panicle showed someeduction for HY8 under AWD, comparing those under CF, butWD significantly increased the percentage of filled grains for thisariety. For LXY18, the number of panicles, spikelets per paniclend the percentage of filled grains were all decreased under AWDompared with those under CF (Table 4).

The irrigation water throughout the growing season was15–305 mm in the AWD regime, which was 44.8–54.6% of that480–560 mm) applied to the CF regime (Fig. 9A). Compared withhat under CF, water productivity (grain yield over the amountf irrigation water and precipitation) under AWD was increasedy 17.7–27.1% for HY8 and 6.3–9.2% for LXY18 (Fig. 9B). Irrigation

ater input and water productivity were greater in 2012 than in

011, which was mainly attributed to less rainfall in 2012 than in011 (refer to Table 1).

able 3oefficients for correlation of root oxidation activity (ROA) and root zeatin (Z) + zeatin ribctivities of sucrose synthase (SuSase), adenosine diphosphate glucose pyrophosphorylas

Variety Correlation with Z + ZR in leaves

HY8 ROA 0.93**

Z + ZR in roots 0.77**

LXY18 ROA 0.97**

Z + ZR in roots 0.89**

a Data used for calculations are from Figs. 7, 8 and 9.** Correlation significant at the P = 0.01 level (n = 16).

al bars represent ± standard error of the mean (n = 3 for Z + ZR content and n = 9 forve the column indicate statistical significance at the P = 0.05 level within the same

4. Discussion

Prior to this study, little information was available describingroot morphology and physiology of WDR and their relationshipswith grain yield and water productivity under both CF and AWDirrigation. Our results showed that a WDR variety had greater rootbiomass, root length density, total root absorption area and activeabsorption area and longer root length and specific root length thana paddy rice variety under AWD, although differences in these roottraits were not significant between the two kinds of varieties underCF conditions (Figs. 3–5). Improvement in these root traits underAWD would contribute to greater shoot biomass and higher grain

Table 4).There is a proposal that a variety that possess a good root pen-

etration ability could maximize soil moisture capture and thereby

oside (ZR) contents with Z + ZR contents in leaves, leaf photosynthetic rate (Pr), ande (AGPase), and starch synthase (StSase) in the grains of rice.a

Pr SuSase AGPase StSase

0.94** 0.90** 0.92** 0.93**

0.84** 0.72** 0.70** 0.74**

0.99** 0.87** 0.88** 0.86**

0.87** 0.73** 0.75** 0.76**

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G. Chu et al. / Field Crops Research 165 (2014) 36–48 45

Fig. 8. Activities of sucrose synthase (A and B), adenosine diphosphate glucose pyrophosphorylase (AGPase) (C and D), and starch synthase (E and F) in grains of the water-saving and drought-resistant rice variety HY8 and paddy rice variety LXY18 under continuous flooding (CF) and alternate wetting and drying (AWD) irrigation in 2011 (A, Cand E) and 2012 (B, D and F). D1 and D2 are measurement time at 90–91 and 101–102 days after transplanting when soil water potential was about −15 kPa in the AWD plot,a ting w( n indic

m2sriti

aprrbaa

nd W1 and W2 are measurement time at 92–93 and 103–104 days after transplann = 3) where these exceed the size of the symbol. Different letters above the colum

aintain a high plant water status under drought conditions (Luo,010; Luo et al., 2011; Yue et al., 2006). We observed that WDRhowed greater root biomass in 11–20 cm soil depth than paddyice under AWD (Table 2), indicating a deeper distribution of rootsn soil for WDR, which would contribute to higher leaf water poten-ial and leaf photosynthesis than paddy rice under water-savingrrigation (Table 2; Fig. 7C and D).

The present results showed that a WDR variety had higher ROAnd Z + ZR content in roots during the soil drying period when com-ared with a paddy rice variety (Fig. 6A–D). Furthermore, ROA andoot Z + ZR content were more increased for WDR than for paddy

ice during the re-watering time. The results imply that WDR have aetter ability to maintain its physiological functions under droughtnd recover functions after the stress, which is hypothesized to bemain physiological trait for a drought-resistant or water-saving

hen plants were re-watered. Vertical bars represent ± standard error of the meanate statistical significance at the P = 0.05 level within the same measurement date.

rice variety (Luo, 2010; Luo et al., 2011; Zou et al., 2007). We arguethat a good root ability to maintain root activity during soil dryingand more recover function during re-watering is another impor-tant physiological reason for WDR to achieve high grain yield andwater productivity under AWD irrigation.

It is proposed that an interdependent relationship existsbetween root and shoot: that is, active shoots that ensure a suf-ficient supply of carbohydrates to roots can develop and maintainactive root functions; the activation of root functions can, in turn,improve shoot characteristics by supplying a sufficient amount ofnutrients, water, and phytohormones to shoots, thus ensures an

increase in crop productivity (Osaki et al., 1997; Yang et al., 2004a,b;Zhang et al., 2009). Herein we observed that root growth wasclosely associated with shoot growth (Figs. 3, 7 and 8), and ROA androot Z + ZR content were very significantly correlated with Z + ZR
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46 G. Chu et al. / Field Crops Research 165 (2014) 36–48

Table 4Grain yield and yield components of the water-saving and drought-resistant rice variety HY8 and paddy rice variety LXY18 under continuous flooding (CF) and alternatewetting and drying (AWD) irrigation.a

Year/variety Irrigation Grain yield (t ha−1) Panicles (per m2) Spikelets (per panicle) Total spikelets (104 m−2) Filled grains (%) Grain weight (mg)

2011HY8 CF 9.58a 275a 164b 4.51a 88.3b 24.4b

AWD 9.34a 270a 161b 4.35a 89.5a 24.5bLXY18 CF 9.67a 258b 170a 4.39a 85.2c 26.7a

AWD 8.55b 243c 162b 3.93b 82.4d 26.5a

2012HY8 CF 9.53a 278a 163b 4.53a 88.4b 24.5b

AWD 9.37a 271a 160b 4.34a 89.7a 24.6bLXY18 CF 9.75a 260b 169a 4.39a 85.4c 26.5a

AWD 8.26b 236c 160b 3.78b 82.7d 26.8a

Analysis of varianceYear (Yr) NSb NS NS NS NS NSVariety (V) 15.4** 21.6** 12.3** NS 9.54** 11.8**

Treatment (T) 43.4** 28.9** 15.7** 9.85** 24.6** NSYr × V NS NS NS NS NS NSYr × T NS NS NS NS NS NSV × T 25.9** 16.5** 11.9** 7.53* 10.5** NS

a Values of grain yield are means of plants of 6 m2 harvested from each plot in each treatment. Values of panicles per m2, spikelets per panicle, total number of spikelets,filled-grain percentage, and filled-grain weight are means of plants harvested from 0.6 m2 from each plot in each treatment. Different letters indicate statistical significanceat the P = 0.05 level within the same column.

b NS, not significant at the P = 0.05 level.* Significant at the P = 0.05 level.

** Significant at the P = 0.01 level.

Fig. 9. Amount of irrigation water (A), and water productivity (grain yield overthe amount of irrigation water and rainfall) (B) of the water-saving and drought-resistant rice variety HY8 and paddy rice variety LXY18 under continuous flooding(CF) and alternate wetting and drying (AWD) irrigation in 2011 and 2012. Verticalbars represent ± standard error of the mean (n = 3) where these exceed the size ofthe symbol. Different letters above the column indicate statistical significance at theP = 0.05 level across the two study years.

content in leaves, leaf photosynthetic rate and activities of SuSase,AGPase and StSase in grains during grain filling (Table 3). Root-sourced cytokinins (Z + ZR) are believed to play a major role inpromoting cell division and delaying senescence (Argueso et al.,2009; Davies, 2004; del Pozo et al., 2005; Yang et al., 2002; Zhanget al., 2010), while SuSase, AGPase and StSase are generally con-sidered as key enzymes involved in sucrose-to-starch conversionin the grains (Fu et al., 2011; Ishimaru et al., 2005; Kato et al.,2007), and their activities are significantly correlated with grainfilling rate or starch accumulation rate in cereals (Hurkman et al.,2003; Yang et al., 2003, 2004a,b; Zhang et al., 2012b). Therefore, wespeculate that improved root morphological and physiological per-formance for WDR benefits shoot physiological processes, leadingto higher grain yield and water productivity under AWD (Table 4,Fig. 9B).

It is noteworthy that there is a report showing a higher grainyield for the super hybrid rice variety Yangliangyou 6 than thatfor the WDR variety Hanyou 3 under AWD conditions (Yao et al.,2012). However, the present study demonstrated a higher grainyield for the WDR variety HY8 than that for the paddy rice varietyLXY8 under AWD (Table 4). The discrepancy between the previousstudy and our work is probably attributed to the difference in use ofrice varieties. Zhang et al. (2012a) observed that the grain yield ofWDR variety HY8 was 17% higher than that of the super rice varietyLiangyoupeijiu under AWD, although it showed no significant dif-ference between the two varieties under CF, in agreement with ourpresent observations. We also observed that, when compared withHanyou 3, HY8 produced 11.5% more grain yield under CF and 14.6%more grain yield under AWD (data not shown). The results suggestthat there are differences in yield potential and drought-resistanceamong WDR varieties and that HY8 has greater yield potential andstronger drought-resistance than Hanyou 3.

It should be also noted that root dry weight in the 0–10 cmsoil layer was a little increased from heading to maturity, though

the total root dry weight in the 0–20 cm soil layer was markedlydecreased during this period (Table 2). The reason for an increasein root dry weight in the 0–10 cm soil layer during grain filling isnot clear. We observed that, in the 0–10 cm soil layer, increases in
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iameter and length per root were more than the decrease in rootumber during the grain filling period (data not shown), whichight lead to an increase in root dry weight. Further research is

eeded by using more rice varieties to investigate root number,oot length, root diameter, and root dry weight in the 0–10 cm soilayer from heading to maturity.

. Conclusion

The WDR variety HY8 produced high grain yield as the cur-ent paddy rice variety LXY18 under CF conditions. Grain yield andater productivity of the WDR variety were significantly higher

han those of the paddy rice variety under AWD. When comparedith paddy rice and under the AWD condition, WDR had better

oot morphological and physiological performance, such as greateroot biomass, root length density, total root absorption area andctive absorption area, longer root length and specific root length,eeper distribution of roots in soil, higher ROA and root Z + ZR con-ent during soil-drying and more increase in root activity duringe-watering. These root traits led to a higher plant water statusnd physiological function during the drought and higher recov-ry function after drought. The improved root morphology andhysiology in WDR could benefit shoot physiological processes,

.e., greater photosynthetic rate and Z + ZR content of/in leavesnd higher activities of key enzymes involved in sucrose-to-starchonversion in grains during grain filling, all which contributed tohigher grain yield and water productivity under water-saving

rrigation.

cknowledgements

We are grateful for grants from the National Basic Research Pro-ram (2012CB114306), the National Natural Science Foundationf China (NSFC-IRRI Joint Research Project 31061140457; Generalroject 31071360; 31271641), the National Key Technology Sup-ort Program of China (2011BAD16B14; 2012BAD04B08), Chinaational Public Welfare Industry (Agriculture) Plan (200803030;01203079), Shanghai Key Project for Agriculture (2010-1-1),iangsu Advantages of Key Construction Projects (JS 2011,),nd Jiangsu Creation Program for Post-graduation StudentsCXZZ13 0902).

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