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Field Crops Research 162 (2014) 30–38

Contents lists available at ScienceDirect

Field Crops Research

jou rn al hom ep age: www.elsev ier .com/ locate / fc r

iomass accumulation and partitioning of newly developed Greenuper Rice (GSR) cultivars under drought stress during theeproductive stage

anuel Marcaida III a, Tao Lia,∗, Olivyn Angelesa, Gio Karlo Evangelistaa,arfel Angelo Fontanillaa, Jianlong Xub, Yongming Gaob, Zhikang Lib, Jauhar Alia,∗

International Rice Research Institute, DAPO 7777, Metro Manila, PhilippinesInstitute of Crop Sciences, Chinese Academy of Agricultural Sciences, 12 South Zhong-Guan-Cun St., Beijing 100081, China

r t i c l e i n f o

rticle history:eceived 17 January 2014eceived in revised form 19 March 2014ccepted 20 March 2014vailable online 12 April 2014

eywords:reen Super Rice

ntrogression breedingrought tolerance mechanismiomass and yield advantage

a b s t r a c t

Drought is a major abiotic threat in rice production; thus, there is a need to develop adaptable rice vari-eties that can withstand drought stress and still produce high yield in non-stressed environments. GreenSuper Rice (GSR) cultivars address this issue. These cultivars are bred through an innovative introgressionbreeding strategy that requires less irrigation water and chemical inputs without compromising grainquality and yield. This study verified the physiological efficiency and performance of newly developed GSRcultivars that previously showed favorable response to drought during advanced yield trials. Five drought-tolerant GSR cultivars and two checks were subjected to continuously flooded (CF) and drought-stressedenvironments during the dry seasons of 2011 and 2012 at the International Rice Research Institute (IRRI)experimental farms in Los Banos, Philippines. The cultivars’ ability to allocate assimilates and accumu-late biomass under drought stress during the reproductive stage was verified. Leaf area index (LAI),biomass dry weight, and panicle yield were measured at the panicle initiation (PI), flowering (FL), andphysiological maturity (PM) of the sample cultivars. All the cultivars performed satisfactorily in the CFenvironment with grain yield ranging from 5 to 11.5 tons ha−1. Water stress during the reproductive stagesignificantly reduced grain yield by 75–88% in the moderate drought (soil water tension between 100 and300 kPa in upper 15 cm soil layer) and 77–96% in the severe drought (soil water tension >300 kPa in upper15 cm soil layer) experiments. The shortened reproductive duration mainly contributed to the significantreduction in yield under drought stress. Two GSR cultivars, GSR IR1-5-S10-D1-D1 and IR83142-B-19-B,responded well in severe drought environments, with grain yield almost similar to the drought check(1.79 tons ha−1). Under moderate drought stress, there was a relative yield advantage of 25% and 40%for the two GSR cultivars over the drought check, respectively. Yield advantage across environments,varying from fully irrigated to drought-stressed, was 31–36%. These two GSR cultivars were effective inmobilizing stored carbohydrates from the vegetative organs to the panicles and not shortening the dura-tion from flowering to maturity, to allow all reserved carbohydrates be allocated to storage organs as amechanism to cope with drought stress. Lower leaf area index (LAI), which allowed balanced biomassaccumulation and lower transpiration, without a significant decrease in grain filling duration, was anotherdrought-coping strategy. These physiological responses and characteristics apparently enabled the GSRcultivars to withstand drought stress; these are key indicators for varietal selection in drought-proneenvironments, particularly in severe drought stress in the reproductive stage. Despite the poor ability of

some cultivars to cope with severe drought, three out of five selected GSR cultivars produced grain yield(2.0–2.9 tons ha−1) that was the same or higher than the drought check in moderate drought stress. Theintrogression breeding technique applied in the newly developed drought-tolerant cultivars through theGSR breeding strategy was found to be effective. It could produce high yields in both CF and water-limited environments, and thus, it cou

∗ Corresponding authors. +63 25805600.E-mail addresses: T.Li@irri.org (T. Li), J.Ali@irri.org (J. Ali).

ttp://dx.doi.org/10.1016/j.fcr.2014.03.013378-4290/© 2014 Elsevier B.V. All rights reserved.

ld serve as a model for other breeding programs to adopt.© 2014 Elsevier B.V. All rights reserved.

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M. Marcaida III et al. / Field

. Introduction

Ninety percent of rice is produced and consumed in AsiaTimmer, 2010; Rejesus et al., 2012) where it is the staple foodf more than 4 billion people. Sustaining a stable rice supply inhe coming years is going to be a challenging task with decreasingources of water, arable land, and fertilizer input. Furthermore, cli-ate change associated with an increasing frequency of extreme

limate events such as drought, floods, and cold or heat wavesdds up another dimension in the existing challenge (Easterlingt al., 2007; Meehl et al., 2007; USGCRP, 2009; CCSP, 2008). Riceeeds to be produced stably without creating production fluctua-ions as experienced during the global food shortage in 2007 and008 (UNCTAD, 2008; FAO, 2010). Among the effects of climatehange, drought is a serious threat to food security, especiallyn rainfed lowlands where 75% of the global rice supply is pro-uced (Maclean et al., 2002). According to Pandey and Bhandari2009), 20% of rice-producing areas in Asia are affected by drought.doption of high-yielding varieties in rainfed areas is constrainedecause farmers are hesitant to take the risk of not applying

rrigation (Lafitte et al., 2007). Also, most of the drought-resistantarieties that have been developed have a lower yield potentialhan high-yielding rice varieties already adopted by the farmersLafitte et al., 2007). Among the rice production constraints thateed immediate attention is the need to develop drought-tolerantarieties suitable for rainfed and irrigated lowlands where droughts going to recur frequently in the coming years (Lafitte et al.,007). It is known that drought occurrence is cyclic in nature andarieties need to perform better in both normal and drought con-itions. Currently, we find very few rice varieties available for suchonditions tha have been developed through conventional breed-ng approaches. Moreover, conventional breeding requires moreime to develop high-yielding, drought-tolerant varieties becausef trait complexities. Among those are the challenges in identify-ng target environments, the interaction of drought tolerance withnvironments, and the availability of the appropriate screeningethodology (Lafitte et al., 2006). An alternative approach has to be

n place to develop new varieties that could cope with the urgencyo produce favorable yield for farmers, whether in drought stressr in fully irrigated conditions. One such method is introgressionreeding as adopted for developing these drought-tolerant mate-ials.

Introgression breeding efforts to identify promising lines thatould survive drought, salinity, and submergence were initiatedn 1998 at the International Rice Research Institute (IRRI) byr. Zhikang Li under the International Rice Molecular Breedingrogram (Li et al., 2005; Ali et al., 2006; Lafitte et al., 2006). How-ver, the work on drought tolerance using an IR64 recipient wasdvanced to design QTL pyramiding and to identify several pyra-iding lines (PDLs) that could withstand severe drought conditions

Guan et al., 2010). Furthermore, research on developing varietieshat could tolerate multiple stresses was initiated in 2008 throughhe Green Super Rice (GSR) breeding strategy. It is an innovativereeding approach that addresses the challenge of making poorarmers benefit from high-yielding varieties with limited resourcesAli et al., 2013).

The Green Super Rice (GSR) breeding program at IRRI haseen successful in developing drought-tolerant cultivars (Ali et al.,012) with yields that are comparable with harvests in favor-ble environmental conditions. The new breeding strategy haseveloped several multiple abiotic stress-tolerant cultivars thatre currently tested under the National Cooperative Testing Tri-

ls in the Philippines. Newly bred GSR lines were developed bycreening BC1F2 bulk populations with Huanghuazhan (HHZ) back-round. They were introgressed from 27 donors to varied abiotictress conditions, including severe drought over three rounds of

Research 162 (2014) 30–38 31

intensive selections, before being nominated to preliminary (twoseasons) advanced yield trials (two seasons). These lines werethen subjected to three stress conditions—drought, irrigated, andlow-nutrient input. Drought lines selected through this innovativebreeding strategy have already shown their relative performance.

More than 87 IRRI-bred GSR lines and 112 CAAS (ChineseAcademy of Agricultural Sciences)-bred GSR materials have beendistributed to national research partners in 16 countries in Asiaand Africa. The GSR materials are also being provided globallythrough IRRI’s International Network for Genetic Evaluation of Rice(INGER), with trials on a regular basis, since 2009. Field trials withGSR cultivars, both in IRRI and Asia, have already demonstratedgood performance in both irrigated and drought conditions (Aliet al., 2012). Development and adoption of high-yielding drought-tolerant cultivars that can withstand severe drought stress andstill produce higher yields in normal conditions (without drought)appear to be a lasting solution in rainfed conditions. There is, then,an urgent need to test the physiological efficiency of these cultivarsand their performances under drought and irrigated conditions.

The improvement of harvest index and increase in dry matteraccumulation were reported as two main factors that enhance riceyield under drought and irrigated conditions (Guan et al., 2010).Moreover, high dry matter accumulation in the reproductive stagealso proved to greatly correlate to high yield under drought. Thestudy of Wu et al. (2008) confirmed that super hybrid rice exhib-ited a greater ability to produce more dry matter and its high yieldmainly resulted from the increase in dry matter accumulation afterthe elongation period. The higher leaf area index and longer leafarea duration contributed to high dry matter production and accu-mulation. It is necessary to confirm whether new IRRI-bred GSRcultivars also possess a similar ability in dry matter production andaccumulation in their high yields.

This study was conducted to understand the difference of newlybred GSR cultivars concerning biomass accumulation, allocation,and yield formation in continuously flooded and drought-stressconditions in comparison with drought-tolerant and irrigated ricecultivars developed from conventional breeding systems.

2. Materials and methods

2.1. Field experiment

This study was carried out during the dry seasons of 2011and 2012 in the experimental farms of IRRI, Los Banos, Laguna,Philippines. Five GSR cultivars with varying levels of toleranceof drought were selected and compared with drought (DC) andirrigated check (IC) varieties (Table 1). These cultivars were pri-marily chosen in order to understand how selection and use of thegiven breeding strategy can influence drought tolerance. They werefound to show favorable response to drought in earlier field trials.Details of the breeding approach adopted to develop the cultivarsare shown in Table 1. The experimental cultivars were subjectedto continuously flooded (CF) and water-limited conditions underpuddled and bunded soils. The former was in a lowland farm with5 cm standing water until 2 weeks before harvest, and the latterwas in an upland farm where drought was applied by withdrawalof irrigation water immediately after 30 days of transplanting, orapproximately before all test cultivars reached panicle initiation(PI), until harvest.

A randomized complete block design was used for the experi-mental plot layout, with three replicates per cultivar for the 2011

experiment and four replicates for 2012. Each replicate plot hasan area of 30 m2 (5 m × 6 m). An area of 5 m2 within each plot wasallotted for destructive sampling on the crop biomass componentsat different phenological stages.

32 M. Marcaida III et al. / Field Crops Research 162 (2014) 30–38

Table 1Characteristic features of GSR cultivars and checks used for CF and drought conditions.

Cultivar Cross information Breeding approach andgeneration

Maturity (days aftersowing) under CF

Description

GSR IR1-12-D10-S1-D1 Huang-Hua-Zhan/Teqing//Huang-Hua-Zhan

Backcross introgressionbreeding BC1F9

110 Aromatic, high-yielding,irrigated cultivar withtolerance of salinity anddrought

GSR IR1-5-S10-D1-D1 Huang-Hua-Zhan/OM1723//Huang-Hua-Zhan

Backcross introgressionbreeding BC1F9

110 High-yielding, irrigatedcultivar with tolerance ofsalinity and drought

GSR IR1-8-S12-Y2-D1 Huang-Hua-Zhan/Phalguna//Huang-Hua-Zhan

Backcross introgressionbreeding BC1F9

110 High-yielding, irrigatedcultivar with tolerance ofsalinity and drought

IR83142-B-19-B IR06G103/IR06G113 Backcross introgressionbreeding and designed QTLpyramiding (DQP)

105 Drought-tolerant pyramidingline

Feng-Fu-Zhan (FFZ) Feng-Si-Zhan/Fu-Qing-Zhan 4 F2 pedigree breeding 115 CAAS-bred GSR variety forirrigated conditions

Irrigated check: PSBRc82 IR47761-27-1-3-6/IRRI 108 F2 pedigree breeding 110 Irrigatedee bre

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mw7mprt2st

Drought check: IR74371-70-1-1 IR55419-4/IR73278 F2 pedigr

In the experiment, 26- and 29-day-old seedlings were trans-lanted to a puddled main field under CF (lowland) and droughtupland) treatments in 2011, respectively. For 2012, the seedlingsere 26 and 24 days old, for CF and drought plots, respectively.

he row and plant spacing was 20 cm × 20 cm with a single planter hill. A separate “trap replicate” was made in the 2011 droughtxperiment, in which the third replicate of the test cultivars wasown a week later to ensure that the effect of drought duringowering is captured fully and evenly for all varieties with one-eek growth duration differences and not allowing drought-stress

voidance to occur. Early flowering genotypes by one week thathowed drought-stress avoidance were anticipated based on pre-ious drought trials in the same site using the same checks.

Nitrogen was applied to CF plots at 160 kg ha−1 with fiveplits—30 kg ha−1 basal; 30 kg ha−1 at 18 days after transplantingDAT) to promote tillering; another 30 kg ha−1 at 33 and 43 DAT;nd finally, 40 kg ha−1 at 64 DAT, which is around PI, to promotepikelet differentiation. The 30 kg ha−1 phosphorus and 30 kg ha−1

otassium fertilizer were applied with basal nitrogen. For therought plots, 30–30–30 NPK fertilizer was applied for basal and0 kg ha−1 of nitrogen was applied at 18 DAT and 33 DAT to fullyatch the growth needs on nitrogen.

.2. Data collection

Five destructive measurements were undertaken at differenttages of the rice growth season: (1) 2 weeks after transplanting14 DAT); (2) 21 DAT; (3) PI; (4) flowering, FL; and (5) physiologi-al maturity, PM. There were 12 hills collected per replicate at eachampling time to measure the leaf area index (LAI); biomass weightf green leaves, dead leaves, stem and panicles; and total above-round biomass weight. The final grain yield was obtained duringarvest.

Tensiometers were installed 15 cm below the soil surface toonitor soil water tension. However, because of the severity ofater stress and because the tensiometers can read only up to

0 kPa, soil water tension was estimated using the ORYZA riceodel (Fig. 1). The 2011 experiment was marked by high tem-

erature and low average rainfall. As such, the 2011 dry season iseferred to as the “severe drought” treatment, at which soil water

ension ranged from 300 to 500 kPa at the reproductive stage. The012 dry season was the “moderate drought” treatment, at whichoil water tension was 100–300 kPa. The average rainfall (Fig. 1) inhe upland farm during the application of drought until harvest was

eding 105 Drought-tolerant varietyrecently released in thePhilippines and India

1.19 and 2.15 mm day−1, with a total rainfall of 71.6 and 155.4 mmduring severe drought (2011) and drought (2012), respectively.

2.3. Data analysis

Using analysis of repeated measures in SAS, the differences indry weight of green leaves, dead leaves, stem, panicles, and totalabove-ground biomass were verified at 5% level of significanceamong the tested cultivars. The performance of each GSR cultivarin specific environment conditions was compared with the checkthrough pair-wise comparisons to verify varietal performance dif-ferences. Dry matter components were converted to percent toverify biomass allocation trends. Analysis of repeated measures andpair-wise comparison with the check was also employed as in thedry weight measurements.

3. Results

3.1. Phenology

Rice plants in drought-stressed conditions during the reproduc-tive stage have shorter growth duration from FL to PM than thosein CF conditions (Table 2). The decrease in duration of the repro-ductive stage positively related to drought severity, that is, a moresevere drought shortened the time from FL to PM even more.

The drought check cultivar IR74371-70-1-1 took a longer timefrom FL to PM, but gave higher panicle yield during drought stress(Table 2). This is also true for two other GSR cultivars with higheryield in water-limited environments—GSR IR1-5-S10-D1-D1 andIR83142-B-19-B.

There was no drought stress during the vegetative phasebecause drought was applied one week before PI. With almost thesame growth conditions in the vegetative stage, the difference induration from transplanting to PI was mainly because of transplan-ting shock resulting from the age of seedlings.

3.2. Leaf area index (LAI)

Water stress significantly decreased LAI relative to cultivar anddrought severity during PI and FL (Table 3). With a pair-wise

comparison between each GSR cultivar and check, a significant dif-ference in the drought experiment was especially observed at FL,but not during PI and PM (Table 3). Four out of five GSR cultivars,which exclude IR1-5-S10-D1-D1, had a significantly lower LAI than

M. Marcaida III et al. / Field Crops Research 162 (2014) 30–38 33

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ig. 1. Amount of precipitation (mm) against soil water tension (kPa) shown in thhaded areas shown in days after sowing (DAS) indicate the period of flowering (FL

he check in severe drought conditions. The opposite was observedn drought conditions, in which all the other GSRs have significantlyigher LAI than the check, except for GSR IR1-5-S10-D1-D1.

No significant difference in LAI was observed at PI among testultivars in severe drought conditions; whereas, IR83142-B-19-Bad a significantly high LAI in drought conditions among all thether cultivars, even significantly higher than the drought check.

able 2henological stage intervals (in days) for the five GSR cultivars under varying levelsf water stress.

Treatment Cultivar Phenology interval (no. of days)a

S-TP TP-PI PI-FL FL-PM

Severedrought(2011)

GSR IR1-12-D10-S1-D1 29 46 32 13GSR IR1-5-S10-D1-D1 29 46 23 22GSR IR1-8-S12-Y2-D1 29 46 26 20IR83142-B-19-B 29 39 27 21FFZ 29 46 34 12Drought check: IR74371-70-1-1 29 32 29 26Irrigated check: PSB Rc82 29 47 31 13

Drought(2012)

GSR IR1-12-D10-S1-D1 24 45 29 23GSR IR1-5-S10-D1-D1 24 40 31 21GSR IR1-8-S12-Y2-D1 24 48 27 25IR83142-B-19-B 24 49 19 24FFZ 24 42 34 16Drought check: IR74371-70-1-1 24 48 20 24Irrigated check: PSB Rc82 24 47 31 13

CF(2011)

GSR IR1-12-D10-S1-D1 26 45 24 28GSR IR1-5-S10-D1-D1 26 39 29 33GSR IR1-8-S12-Y2-D1 26 45 27 26IR83142-B-19-B 26 34 29 33FFZ 26 43 25 36Drought check: IR74371-70-1-1 26 31 27 31Irrigated check: PSB Rc82 26 44 25 29

CF(2012)

GSR IR1-12-D10-S1-D1 22 44 25 26GSR IR1-5-S10-D1-D1 22 42 25 28GSR IR1-8-S12-Y2-D1 22 40 24 31IR83142-B-19-B 22 37 23 29FFZ 22 43 25 28Drought check: IR74371-70-1-1 22 43 25 32Irrigated check: PSB Rc82 22 35 23 31

a S-TP = sowing to transplanting; TP-PI = transplanting to panicle initiation; PI-L = panicle initiation to flowering; FL-PM = flowering to physiological maturity.

ght experiment from the start of irrigation withdrawal until harvest whereas thee test cultivars.

3.3. Partitioning of assimilates

Accumulation of biomass in CF and water-limited experimentswas not significantly different among the test cultivars. Differencesin the partitioning of assimilates during the reproductive phase wasnotable because water stress was applied thereafter, a week beforePI. As was expected, the samples in CF environments producedgreater biomass yield, having received the necessary water require-ments. In 2011, total biomass from PI to PM was 42–70% lower insevere drought than that in CF plots; whereas, it was 10–20% lowerin 2012 with drought stress (Tables 4 and 5).

In severe drought conditions in 2011, no significant difference

was found in the assimilate partitioning in different plant organsfrom PI to FL among the GSR cultivars (Tables 4 and 5). Pair-wise comparison with check did not show a significant differencein biomass allocation at PI. At FL, most of the GSR cultivars had

Table 3Leaf area index (LAI) of GSR cultivars compared with check under droughtconditions.

Treatment Cultivar PI FL PM

Severedrought

GSR IR1-12-D10-S1-D1 1.27 1.08bc* 0.26GSR IR1-5-S10-D1-D1 1.44 2.38a 0.31GSR IR1-8-S12-Y2-D1 1.65 1.02c* 0.52IR83142-B-19-B 1.34 1.48abc* 0.11FFZ 1.73 1.21abc* 0.39Drought check 0.89 2.19ab 0.18

Drought GSR IR1-12-D10-S1-D1 1.65ab 2.74ab* 0.93*GSR IR1-5-S10-D1-D1 0.65b 1.93ab 0.46GSR IR1-8-S12-Y2-D1 1.13ab 2.24ab* 0.32IR83142-B-19-B 2.17a* 2.26ab* 0.24FFZ 1.34ab 3.07a* 0.90*Drought check 1.42ab 2.52b 0.54

CF (2011and 2012average)

GSR IR1-12-D10-S1-D1 3.42 5.28 1.62ab*GSR IR1-5-S10-D1-D1 3.72 4.42 1.35abGSR IR1-8-S12-Y2-D1 3.45 5.03 2.13a*IR83142-B-19-B 3.63 4.89 0.62bFFZ 3.77 5.49 1.17abIrrigated check 3.57 5.16 0.88ab

In a column, means followed by the letters a, b, and c denote significant differenceat 5% level by LSD; whereas, means followed by the symbol * denote significantdifference from the check at 95% probability.

34 M. Marcaida III et al. / Field Crops Research 162 (2014) 30–38

Table 4Biomass allocation (%) of GSR cultivars and checks in drought-stressed environments during the reproductive stage.

Biomass Cultivar 2011 severe drought stress (%) 2012 drought stress (%)

PI FL PM PI FL PM

Panicles GSR IR1-12-D10-S1-D1 0 6 25c* 0 17 45c*GSR IR1-5-S10-D1-D1 0 12 36ab 0 12 52abGSR IR1-8-S12-Y2-D1 0 8 5c* 0 11 27c*IR83142-B-19-B 0 14 41a 0 19 52abFFZ 0 12 19bc* 0 18 43bc*Drought check 0 14 37a 0 17 54a

Greenleaves

GSR IR1-12-D10-S1-D1 40 21 11ab 35 20 8a*GSR IR1-5-S10-D1-D1 52 22 8ab 33* 20 3abGSR IR1-8-S12-Y2-D1 40 19* 16a* 32* 16 6ab*IR83142-B-19-B 56 17* 4ab 33* 17 1abFFZ 43 17* 12ab* 35 20 6ab*Drought check 44 23 5b 35 18 2b

Stem GSR IR1-12-D10-S1-D1 60 53 66b 47 51b 41bGSR IR1-5-S10-D1-D1 48 43 62ab 49 56ab 37bGSR IR1-8-S12-Y2-D1 60 69 67a* 54* 64a* 54a*IR83142-B-19-B 44 42 64ab 51* 54ab 40bFFZ 57 56 64ab 49 51b 42bDrought check 56 43 60ab 49 55ab 36b

Deadleaves

GSR IR1-12-D10-S1-D1 0 6* 12b* 18 11 7GSR IR1-5-S10-D1-D1 0 4 13ab 18* 12 7GSR IR1-8-S12-Y2-D1 0 6* 11ab* 15 8 12*IR83142-B-19-B 0 4 13a 17 11 7FFZ 0 6 12ab 16 10 9Drought check 0 3 15ab 16 10 8

I t 5% lef

aSltdtt

e

TD

As

n a column, means followed by the letters a, b, and c denote significant difference arom the drought check at 95% probability.

significantly higher stem biomass, except for GSR IR1-12-D10-1-D1, which had no significant difference with the check. Deadeaf biomass of all the GSR cultivars was significantly higher thanhat of the drought check. “Trap replicates” experienced the severerought before reaching FL that resulted to a longer duration for PI

o FL and lower biomass. Some varieties in this replicate even failedo reach grain filling.

In the 2012 drought experiment, there was a significant differ-nce between the amount and percentage of assimilates allocated

able 5ry matter accumulation and partitioning (kg ha−1) of GSR cultivars at the reproductive s

Cultivar/treatment PI (kg ha−1) FL (kg ha−1)

GL DL ST PAN TB GL DL

Severe droughtGSR IR1-12-D10-S1-D1 653 0 975 0 1628 719 20GSR IR1-5-S10-D1-D1 641 0 582 0 1223 997 17GSR IR1-8-S12-Y2-D1 661 6 996 0 1663 682 22IR83142-B-19-B 590 0 473 0 1063 785 20FFZ 922* 0 1230 0 2151 768 28Drought check 504 0 638 0 1141 767

DroughtGSR IR1-12-D10-S1-D1 902 451 1215 0 2568 1200a* 64GSR IR1-5-S10-D1-D1 645 362 975 0 1982 985ab* 5GSR IR1-8-S12-Y2-D1 725 334 1222 0 2282 1326a* 67IR83142-B-19-B 1069* 538* 1648* 0 3255* 980ab* 61FFZ 699 321 996 0 2016 1321a* 68Drought check 731 339 1034 0 2103 713b 3

CF (2011)GSR IR1-12-D10-S1-D1 1349 6 1571 0 2926 2862

GSR IR1-5-S10-D1-D1 1377 7 1606 0 2990 3165

GSR IR1-8-S12-Y2-D1 1667 12 2040 0 3719 3073

IR83142-B-19-B 812 8 1080 0 1899 2404*

FFZ 1313 9 1495 0 2817 3082

Irrigated check 1421 15 1499 0 2935 3003

CF (2012)GSR IR1-12-D10-S1-D1 920 0 1229 0 2149 1689 76GSR IR1-5-S10-D1-D1 1112 0 1508 0 2620 1334 8GSR IR1-8-S12-Y2-D1 1292 0 2184 0 3476 1891 9IR83142-B-19-B 1093 0 1967 0 3060 1550 75FFZ 898 0 961 0 1859 1714 8Irrigated check 1114 0 1352 0 2466 1694 9

ssimilate partitions: GL = green leaves, DL = dead leaves, ST = stem, PAN = panicles, and

ignificant difference at 5% level by LSD; whereas, means followed by the symbol * denot

vel by LSD; whereas, means followed by the symbol * denote significant difference

to the stem and green leaves, but no significant difference on pani-cle biomass at FL (Table 4). Significant differences were noticeableduring FL, in which leaf and stem assimilates of the GSR culti-vars were almost always higher than IR74371-70-1-1, the droughtcheck. Only GSR IR1-5-S10-D1-D1 showed no significant difference

in stem and dead leaf biomass as compared with the check. For GSRIR1-8-S12-Y2-D1 and FFZ, green leaf and stem biomass were higherthan the check and comparable to other GSR cultivars. On the otherhand, panicle biomass was lower at PM, indicating failure to deliver

tage under drought, severe drought, and CF conditions.

PM (kg ha−1)

ST PAN TB GL DL ST PAN TB

9* 2208 207 3343 350ab 388 1702b 795ab* 32352* 2852* 565 4586 352ab 592 1928ab 1606a 44789* 2466* 281 3658 748a* 504 3263a* 248b* 47634* 2987* 671 4647 178b 612 1954ab 1916a 46605* 2805* 531 4388 520ab* 518 2409ab 829ab* 427688 1946 468 3269 179b 559 1672b 1437a 3846

5* 3013bc* 997 5855abc* 524a* 465b 2734b 3026ab 674868 2740bc 581 4874bc 221ab 477b 2376b 3350a 64257* 5196a* 905 8104c* 469ab* 880ab* 3945a* 1956b* 7250*5* 3156bc* 1086 5837abc* 73b 446b 2555b 3328a 64016* 3399b* 1221 6626ab* 396ab* 543ab 2627b 2686ab 625291 2148c 685 3938c 133ab 432b 2048b 3012ab 5625

38 4541 1415 8855 1859ab* 660b* 4622 7249a 14,38935 4876 1723 9800 1548ab 872ab* 4105 7019a 13,54381 5165 1326 9644 1925a* 653b* 5012* 5040b* 12,63051 4431* 1483 8369 856b 964ab* 3963 7050a 12,83350 5580 1784 10496 1696ab* 930ab* 4893* 7925a* 15,445*63 4617 1650 9333 1112ab 1470a 4026 6741a 13,349

9* 3323 1119 6900 91 1477* 1192 5418a 817808 3193 1345 6680 134* 1591* 1201 5106a 803261 4463 1602 8917 76 2247* 1500* 5770b* 9593*5* 3336 843* 6483* 54 1503* 936 4852a 734589 3208 1217 7028 36* 1723* 1473 5880a* 9111*03 3381 1322 7299 70 858 949 4599a 6476

TB = total biomass. In a column, means followed by the letters a, b, and c denotee significant difference from drought check at 95% probability.

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arbohydrates to the storage organ or a lower transferring capabil-ty of reserved soluble carbohydrates from stem to panicle from FLo PM.

There was no significant difference in the total biomass duringM across cultivars in two drought environments. Under CF con-itions, GSR IR1-8-S12-Y2-D1 and FFZ gave a significantly higherotal biomass than all other cultivars.

Upon reaching PM, IR83142-B-19-B and GSR IR1-5-S10-D1-D1howed more promising performance than other GSR cultivars,ith consistently high panicle yield in both CF and water-stressed

nvironments (Tables 4 and 5). Both cultivars gave a panicle yieldf at least 1.5 tons ha−1 and 35% dry mass allocated to panicles inevere drought conditions (2011), which was 12–33% higher thanhe drought check. In the 2012 drought conditions, the panicle yieldf both cultivars was at least 3.3 tons with dry mass allocation tohe panicles 52% of the total above-ground biomass (TB). Panicleiomass thaw was 10–11% higher than that of the drought check.anicle yield under CF conditions ranged from 5 to 7 tons ha−1, withanicle biomass of 52–66% of TB. By ANOVA and pair-wise compari-on, however, the advantage in panicle biomass shown by these twoSR cultivars was not significant compared to the check varieties

Table 5).Plant materials with low percentage of green leaf biomass at PM

ave relatively higher proportions of panicle biomass as in the casef IR83142-B-19-B and GSR IR1-5-S10-D1-D1 (Table 4). The oppo-ite is true for GSR IR1-8-S12-Y2-D1, which has the highest totalbove-ground biomass at PM in the two drought environments,ut has the lowest panicle yield among all the other GSR culti-ars. These GSR cultivars, including GSR IR1-12-D10-S1-D1 and FFZ,ave a high amount and percentage of assimilates in green leavesnd stem, indicating their failure to efficiently deliver the reservedoluble carbohydrates to the reproductive organs in water-limitedonditions (Tables 4 and 5). The shorter duration from FL to PM,mplying short duration for grain filling, also contributed to low-ielding GSR cultivars under drought stress (Tables 2 and 5).

Grain yield was measured upon harvest and shown in Table 7.ield in irrigated plots ranged from 5 to 7.9 tons ha−1 in 2011nd from 6.6 to 11.5 tons ha−1 in 2012. As observed at PM inoth drought environments, cultivars in severe drought stress gave

ower grain yield (0.28–1.67 tons ha−1) than those in moderaterought stress (1.28–2.91 tons ha−1), with IR83142-B-19-B and GSR

R1-5-S10-D1-D1 consistently showing higher yield than the otherultivars. In comparison with the check varieties, grain yield ofSR cultivars was higher in the 2011 irrigated environment. Thepposite was observed in 2012, in which the check variety hadigher grain yield than all the GSR cultivars except for GSR IR1-10-S1-D1. In the water-limited environment, results showed that

he check variety had higher grain yield than all the GSR varietiesnder severe drought conditions (2011). While GSR IR1-5-S10-D1-1 and IR83142-B-19-B have a relatively higher grain yield than

he check, all the other GSR cultivars have close but lower grainield than the check.

. Discussion

In the dry seasons of 2011 and 2012, drought environmentsere created after irrigation was stopped. Slow elongation of

tems, steep leaf angle, short plant height, and leaf-rolling, whichanifested in the decreased LAI and biomass weight, were

bserved more in the GSR cultivars under drought than under CFTables 3 and 5). These indicate that the GSR cultivars have simi-

ar drought coping mechanisms as commonly observed for plantsubjected to drought stress to avoid dehydration and completeheir life cycle (Wopereis et al., 1996; Chaves et al., 2003). The cru-ial and severe effect of drought stress in rice happens during the

Research 162 (2014) 30–38 35

reproductive and grain-filling stages while reserved carbohydratesin vegetative organs are translocated to the panicles. Boonjung andFukai (1996) reported that the inability of leaves and stems to effec-tively deliver stored carbohydrates to the storage organs causes lowyield.

Since no significant difference was observed in all the experi-mental plots during the vegetative stage when drought stress wasnot yet applied, the discussions herein focus mainly on the parti-tioning of assimilates from PI to PM. The differences in assimilatepartitioning and growth-stage duration defined the ability of GSRto cope with drought stress as shown by the panicle yield of thecultivars.

There was an obvious decline in biomass yield compared to CFtreatments in the reproductive stage when drought was applied. Itis necessary to examine the biomass accumulation and assimilatepartitioning behavior that enabled the well-performing GSR culti-vars to cope with stress brought about by limited water availabilityand still produce high panicle and grain yield (Tables 4 and 7).To examine the behavior of the GSR cultivars together with thedrought check, biomass production rate analysis was employed.

The rate of biomass production (kg ha−1 day−1) is an estimateof the amount of biomass productivity between two phenologicalstages. It is computed by getting the difference in biomass weightbetween two phenological stages divided by the stage duration (indays). A positive value represents an increase in the rate of biomassformation, whereas a negative value indicates a decrease in the rateof biomass production resulting from leaf death or translocation ofcarbohydrates to the panicles and the burning of carbohydratesto survive the drought (Table 6). As in the study of Boonjung andFukai (1996), variation in biomass produced during specific growthstages affects the grain yield.

When the rice plants reach FL, the carbohydrates stored in thevegetative organs are delivered to the panicles until PM. There-fore, it is important to realize that the biomass produced in theleaves and stem from the vegetative stage to PI is needed to buildup enough sources for translocation. Table 6 shows the transloca-tion (by the vegetative organs) and accumulation (by the storageorgans) of assimilates from FL to PM. It is noticeable how biomassin the leaves and stem drastically decreased from FL to PM in thedrought experiments. This mechanism is indicative of the plant’scoping strategy at the sense of water stress, thereby producingreserves to be able to mobilize itself for panicle production duringgrain filling (Barnabas et al., 2008; Chaves et al., 2003; Yang andZhang, 2006). Efficient translocation is indicated by the high accu-mulation rate of the panicle and more negative values for the leavesand stem (Table 6). The negative production rates of the stem andleaves of GSR IR1-12-D10-S1-D1, GSR IR1-5-S10-D1-D1, IR83142-B-19-B, and FFZ indicate delivery of carbohydrates to the paniclesfrom FL to PM. The opposite was observed for GSR IR1-8-S12-Y2-D1, in which it continued to accumulate reserves in the vegetativeorgans but failed to translocate them, thus it has the lowest pani-cle and grain yield in severe drought stress (2011). Its panicle andgrain yield were also the lowest in moderate drought stress (2012)because of low translocation coefficient, although reserves wereused for grain filling (Tables 5 and 7).

Comparing the delivery of carbohydrates during PI to FL(Table 6) showed a rate of assimilate accumulation almost simi-lar in the leaves and stem during PI to FL in the 2011 and 2012experiments. The drought experiment in 2012 showed that GSRcultivars can produce a panicle yield of at least 2 tons ha−1 (Table 5)under moderate drought (100–300 kPa) through their efficiency intranslocating carbohydrates to the panicles from FL to PM.

As shown in studies by Yang and Zhang (2006) and Boonjung andFukai (1996), the time to reach maturity was shortened as observedin poorly performing GSR cultivars (Table 2), and it was very appar-ent in severe drought. Water stress during grain filling could hasten

36 M. Marcaida III et al. / Field Crops Research 162 (2014) 30–38

Table 6Rate of biomass accumulation in five GSR cultivars under three different crop growth conditions.

Cultivar/treatment PI-FL (kg ha−1 day−1) FL-PM (kg ha−1 day−1)

TL ST PAN TB TL ST PAN TB

Severe droughtGSR IR1-12-D10-S1-D1 8 38 6 52 −15 −40 46 −9GSR IR1-5-S10-D1-D1 24 100 25 149 −10 −41 47 −4GSR IR1-8-S12-Y2-D1 10 57 11 78 17 41 −2 56IR83142-B-19-B 15 93 25 133 −10 −49 59 0FFZ 3 46 16 63 −1 −34 26 −9Drought check 12 45 16 73 −5 −11 37 −21

DroughtGSR IR1-12-D10-S1-D1 17 62 34 113 −38 −12 89 39GSR IR1-5-S10-D1-D1 18 58 19 95 −40 −17 130 73GSR IR1-8-S12-Y2-D1 36 150 34 220 −27 −51 42 −36IR83142-B-19-B −1 79 57 135 −45 −25 93 23FFZ 29 71 36 136 −69 −50 94 −25Drought check 2 56 34 92 −22 −4 97 71

CF (2011)GSR IR1-12-D10-S1-D1 63 122 58 243 −14 3 208 197GSR IR1-5-S10-D1-D1 63 113 59 235 −24 −24 162 114GSR IR1-8-S12-Y2-D1 55 116 49 220 −22 −6 143 115IR83142-B-19-B 55 114 51 220 −19 −14 170 137FFZ 73 163 71 307 −14 −19 171 138Irrigated check 66 126 67 259 −16 −20 174 138

CF (2012)GSR IR1-12-D10-S1-D1 60 83 44 187 −34 −82 165 45GSR IR1-5-S10-D1-D1 42 68 54 164 −14 −71 133 48GSR IR1-8-S12-Y2-D1 65 95 67 227 −18 −96 134 20IR83142-B-19-B 53 59 36 148 −26 −83 139 30FFZ 69 90 49 208 −31 −63 170 76Irrigated check 66 90 59 215 −53 −78 106 −25

A tal bP

mte1tltftull

Sl(ci(hw

TG

T

ssimilate partitions: TL = leaves (green + dead), ST = stem, PAN = panicles, TB = toM = flowering to physiological maturity.

aturity. In favorable and non-resource-limited environments, theime between flowering to maturity takes at least 30 days; how-ver, it was cut short into at least 12 days in severe drought and6 days in drought conditions. On the contrary, the drought checkogether with GSR IR1-5-S10-D1-D1 and IR83142-B-19-B took aonger time (21–26 days), allowing them to have a long period forranslocation of carbohydrates and for generation of assimilates toacilitate grain filling. In contrast, GSR IR1-12-D10-S1-D1 and FFZried to cope with drought stress by speeding up maturity, but werensuccessful in delivering as much assimilates to the panicles. This

owered translocation efficiency relative to those under CF, thus theow panicle yield at PM.

Among the five GSR cultivars used in this study, GSR IR1-5-10-D1-D1 and IR83142-B-19-B were able to withstand differentevels of water stress with 1.6–3.3 tons ha−1 of panicle yield at PMTable 5), and 1.3–2.6 tons ha−1 of grain yield at harvest. These twoultivars distinctly had the ability to effectively translocate assim-

lates stored in the vegetative organs from previous growth stagesTable 6). Furthermore, high translocation was facilitated by notaving to dramatically cut short their grain-filling duration, unlikeith other cultivars (Table 2).

able 7rain yield of GSR cultivars and checks at harvest.

Cultivar Irrigated

2011 2012

GSR IR1-D10-S1-D1 7.25 (+7.6) 11.48

GSR IR1-S10-D1-D1 7.02 (+4.2) 10.35

GSR IR1-8-S12-Y2-D1 5.04 (−25.2) 10.53

IR83142-B-19-B 7.05 (+4.6) 10.52

FFZ 7.93 (+17.7) 10.74

Irrigated check 6.74 11.31

Drought check 5.78 6.56

he figures in parenthesis are yield differences relative to the check (i.e., irrigated check u

iomass. Phenological stage intervals: PI-FL = panicle initiation to flowering, FL-

Under severe drought, IR83142-B-19-B was able to sustain itsphotosynthetic activity and effectively translocate carbohydratesto the panicles as manifested by the lack of significant change inTB from FL to PM (Table 5). Low LAI under moderate drought stress(Table 3) allowed low water requirements for transpiration andphotosynthesis; hence, photosynthesis is more effective per unitarea of LAI with no significant difference in TB among GSR culti-vars. In the case of GSR IR1-5-S10-D1-D1 under severe drought, inwhich LAI is relatively higher (Tables 3 and 5), the product of pho-tosynthesis was adequate for plant maintenance. Thus, there wasno significant change in TB from FL to PM (i.e., growth rate of TBalmost 0). Both cultivars (IR83142-B-19-B and GSR IR1-5-S10-D1-D1), with enough carbohydrates produced from photosynthesis,have a very efficient translocation ability that enabled them tocope with different drought-stress conditions, and this is why theyperformed better than the other GSR cultivars.

Comparing panicle yield at PM with the drought check under

moderate drought stress, there was no significant differenceobserved in four GSR cultivars—GSR IR1-12-D10-S1-D1, GSR IR1-5-S10-D1-D1, GSR IR1-8-S12-Y2-D1, and FFZ (Table 5). Thesecultivars are able to produce a panicle yield of 3.3 tons ha−1

Drought

2011 2012

(+1.5) 0.46 (−74.3) 2.03 (−2.4)(−8.5) 1.30 (−27.4) 2.60 (+25.0)(−6.9) 0.28 (−84.3) 1.28 (−38.5)(+7.0) 1.67 (−6.7) 2.91 (+40.0)(−5.0) 0.81 (−54.7) 1.98 (−4.8)

1.29 2.681.79 2.08

nder irrigated conditions and drought check under drought-stressed conditions).

M. Marcaida III et al. / Field Crops Research 162 (2014) 30–38 37

Table 8Multi-environment and multi-treatment yield of GSR cultivars in DS 2011 and 2012.

Cultivars Seasonal meana (tons ha−1) Mean by treatmentb (tons ha−1) Varietal mean across seasonsand treatmentsc (tons ha−1)

Percent advantage overdrought check

2011 2012 Irrigated Drought

GSR IR1-12-D10-S1-D1 3.86 6.76 9.37 1.25 5.31 31.1GSR IR1-5-S10-D1-D1 4.16 6.48 8.69 1.95 5.32 31.4GSR IR1-8-S12-Y2-D1 2.66 5.91 7.79 0.78 4.28 5.7IR83142-B-19-B 4.36 6.72 8.79 2.29 5.54 36.8FFZ 4.37 6.36 9.34 1.4 5.37 32.6Irrigated check 4.02 7 9.03 1.99 5.51 36.0Drought check 3.79 4.32 6.17 1.94 4.05 –

ts com expeasons

a1e

Idra

e(dacawShhdymc

iGgago

atr

ofatlgav

5

oIe

a Seasonal mean is the average grain yield of the irrigated and drought treatmenb Mean by treatment is the average grain yield for each treatment during the twoc Varietal mean is the average grain yield of each cultivar with treatments and se

nd grain yield of 2.6–2.9 tons ha−1 at a soil water tension of00–300 kPa, hence, they can be recommended for drought-pronenvironments.

When compared to the drought check, the grain yield ofR83142-B-19-B and GSR IR1-5-S10-D1-D1 was lower in severerought and not significantly higher in moderate drought envi-onments. However, these two cultivars continue to show yielddvantage over the other GSR samples.

Resilience of GSR cultivars could be ascertained by making anffective comparison on (1) the mean grain yield across seasonsDS 2011 and 2012), from which the average of the irrigated androught experiments were obtained; (2) the treatment (irrigatednd drought), in which the 2-year means of each treatment wasomputed; and (3) the mean varietal performance across seasonsnd treatments (Table 8). Regardless of the variability of seasonaleather and the availability of water, the cultivars GSR IR1-5-

10-D1-D1 and IR83142-B-19-B were fairly consistent in obtainingigh grain yield of 2.0–8.8 tons ha−1 and were comparable and/origher than the checks. In typical rainfed lowland situations in Asia,rought does not recur each year with the same intensity; someears may have favorable seasons. Therefore, varieties need to beore resilient and should have a relatively high yield in all such

onditions (Lafitte et al., 2006).For the yield average of the drought and irrigated experiments

n 2011 (Table 8), when the drought stress was more severe, all theSR varieties gave a yield of at least 2.5 tons ha−1. Three cultivarsave higher yield than the irrigated and drought checks. In 2012,ll the GSR varieties have a higher yield than the drought check,iving a combined average yield from irrigated and drought plotsf 5.9–6.7 tons ha−1.

The mean of each treatment from two seasons (Table 8) onlyffirm earlier findings about the varieties that perform well andhe ability of GSR to produce high yield in non-water-limited envi-onments.

The multi-environment mean in Table 8 showed the resiliencyf GSR cultivars, having been exposed to two dry seasons in two dif-erent environments (water-limited and irrigated). While they gavelmost the same yield as the irrigated check, all the grain yields ofhe GSR cultivars, which ranged from 4.3 to 5.5 tons ha−1, were ateast 5.7–36.7% higher than the drought check. This indicates that,iven the unpredictability of weather conditions in rice-producingreas every year, in the presence or absence of drought, GSR culti-ars are capable of producing high grain yield in the long run.

. Conclusions

With the introduction of water stress before the onsetf the reproductive stage, GSR entries IR1-5-S10-D1-D1 andR83142-B-19-B were able to withstand drought of varying lev-ls, thereby producing grain yield of 1.1–2.9 tons ha−1. These two

bined for each season.rimental seasons.

combined.

drought-tolerant GSR cultivars did not have to abruptly shortentheir duration from FL to PM, compared with other GSR test mate-rials, to reduce the grain-filling period in order to cope with waterlimitation. This could have allowed efficient translocation of assimi-lates and reserved carbohydrates from the vegetative organs to theultimate sink (panicle yield). Low LAI enabled balanced biomassaccumulation with low transpiration, preventing significant reduc-tion in grain filling.

GSR tolerant cultivars subjected to 100–300 kPa of water stresswere able to deliver more products of photosynthesis and storedcarbohydrates to the panicles than those under severe water stress,and were able to produce 2.0–3.3 tons ha−1 of panicle yield.

This study also showed that introgression breeding employedin GSR was successful in developing drought-tolerant cultivars.Although not expressed well by all the GSR cultivars under severedrought conditions (soil tension higher than 300 kPa at 15-cm soildepth), those cultivars that did not perform well under severedrought stress could have salinity and flooding tolerance besidesmoderate drought tolerance and there exists a compensationmechanism when materials are selected for multiple abiotic stressconditions. Grain yield of at least 2 tons ha−1 could be expectedfrom GSR cultivars in moderate drought conditions with soil watertension of 100–300 kPa at a 15-cm depth. Multi-environment com-parison also showed the resiliency of the GSR cultivars, therebyproducing an average grain yield of 4.3–5.5 tons ha−1 in two dryseasons, with yields from drought and irrigated environments com-bined.

Acknowledgments

The funds for this research were provided under the GreenSuper Rice Project “GD1393-1” by Bill & Melinda Gates Foundationthrough Chinese Academy of Agricultural Sciences (CAAS), Beijingto the International Rice Research Institute, Philippines.

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