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Dry matter production in relation to root plastic development, oxygen

transport, and water uptake of rice under transient soil moisture stresses

Article in Plant and Soil · July 2010

DOI: 10.1007/s11104-009-0275-8

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Plant Soil (2010) 332:87–104
DOI 10.1007/s11104-009-0275-8

REGULAR ARTICLE

Dry matter production in relation to root plastic

development, oxygen transport, and water uptake of rice
under transient soil moisture stresses
Roel Rodriguez Suralta & Yoshiaki Inukai &
Akira Yamauchi

Received: 15 September 2009 / Accepted: 23 December 2009 / Published online: 27 January 2010
# Springer Science+Business Media B.V. 2010

Abstract Drought and waterlogging are important greater shoot dry matter production than Nippon-
abiotic stresses negatively affecting plant growth bare. This was due largely to its greater root system
and development. They are transiently recurring in development through high induction of aerenchyma
rainfed lowlands and in water-saving system prac- formation. Consequently, aerenchyma development
ticing intermittent irrigation. This study aimed to effectively facilitated the internal diffusion of oxy-
determine the contribution of plastic development gen (O2) to the root tips under sudden waterlogged
and associated physiological responses of roots to condition supporting rapid recovery of stomatal
shoot dry matter production under transient soil conductance, transpiration, and photosynthesis.
moisture stresses. To minimize effect of genetic Likewise, CSSL47 showed greater shoot dry matter
confounding, a selected line (CSSL47) drawn from production than Nipponbare under transient
54 chromosome segment substitution lines (CSSL) waterlogged-to-droughted (W–D) conditions. This
of Nipponbare (japonica type) carrying an over- was due to CSSL47’s greater root system develop-
lapping chromosome segments of Kasalath (indica ment through more initiation of L type lateral roots
type), was used and compared with the recurrent that effectively maintained soil water uptake. This in
parent Nipponbare. Under transient droughted-to- turn sustained higher stomatal conductance, transpi-
waterlogged (D–W) conditions, CSSL47 showed ration, and photosynthesis. Results implied that
utilization of CSSLs could precisely reveal that root
plastic development in response to transient soil
moisture stresses contributed to the maintenance of
Responsible Editor: Len Wade. shoot dry matter production.
R. R. Suralta
Agronomy, Soils, and Plant Physiology Division, Keywords Aerenchyma . Drought . Lateral roots .
Philippine Rice Research Institute (PhilRice), Oxygen transport . Waterlogging . Water use
Science City of Muñoz,
Nueva Ecija 3119, Philippines
Abbreviations
Y. Inukai : A. Yamauchi (*) CSSL chromosome segment substitution line
Graduate School of Bioagricultural Sciences, DAS days after sowing
Nagoya University,
Chikusa,
D-W droughted-to-waterlogged
Nagoya 464-8601, Japan SMC soil moisture content
e-mail: [email protected] W–D waterlogged-to-droughted
88 Plant Soil (2010) 332:87–104

Introduction preceding soil moisture stress (i.e. drought or

waterlogging) prior to encountering the succeeding
Drought and waterlogging are two of the most contrasting soil moisture stress (i.e. droughted-to-
important abiotic stresses negatively affecting plant waterlogged or waterlogged-to-droughted transi-
growth and development. In this aspect, it is impor- tion). Hence, rice plants require different root
tant to understand that these soil moisture stresses system development strategies for adaptation. The
transiently recur in the field due to the intermittent extent of the contribution of root plastic develop-
nature of rainfall patterns and irrigation systems. ment is difficult to assess under fluctuating soil
Hence, the soil is exposed to frequent episodes and moistures, as both the constitutive and adaptive root
varying degrees of alternate dry and wet conditions trait responses are present and each interacts with
causing transient drought and O2 deficiency to plants. both the existing conditions and the genotypic
The inability of plant to acclimate to such changes background of the diverse cultivars used (Kamoshita
may result in reduced growth and dry matter et al. 2002a). These interactions consequently limit
production. However, most of the studies in the past precise phenotyping for identification of relevant
dealt only on the effects of either of the stresses QTLs (Kamoshita et al. 2002b). The constitutive
(Wang and Yamauchi 2006). Little attention has been root traits are expressed under favorable anaerobic
devoted to their interactive effects. conditions. The adaptive root traits require water
A series of our previous studies provided stress for their expressions (e.g., promoted root
evidence that changing soil moisture conditions elongation rate and plastic lateral root production;
adversely affect crop root development mainly by Bañoc et al. 2000b, and enhanced aerenchyma under
reducing root elongation and branching into lateral sudden waterlogged conditions; Justin and Armstrong
roots, and these limit for soil water uptake ability, 1987).
which then results in reduced stomatal conductance, In our previous study in rice (Suralta et al.
transpiration and photosynthesis. Ultimately, this 2008a), we found that aerobic cultivars have greater
results in reduced shoot dry matter production ability for plastic lateral root production than
(Bañoc et al. 2000a, b; Pardales and Yamauchi irrigated lowland cultivars under transient moisture
2003; Siopongco et al. 2008, 2009; Subere et al. stresses. Specifically, greater ability for plastic
2009; Wade et al. 2000; Yamauchi et al. 1996). lateral root production in aerobic than irrigated
Cognizant of this, the ability of roots to respond to lowland cultivars were due to the aerobic cultivars’
these fluctuating soil moisture regimes was proposed ability to maintain higher rate of seminal root
as one of the important developmental traits for elongation and more number of nodal and lateral
adaptation (Ingram et al. 1994; Wang and Yamauchi roots in response to transient O2 deficient-to-drought
2006; Yamauchi et al. 1996). Under progressive soil conditions, and higher rate of seminal root elonga-
drying, root responses include increased root length tion, more aerenchyma formations in the seminal
density (Siopongco et al. 2005) as a result of plastic root axis, and more number of nodal roots in
lateral root development (Azhiri-Sigari et al. 2000; response to transient droughted-to-O2 deficient
Bañoc et al. 2000b; Kamoshita et al. 2000). On the conditions.
other hand, development of shallow root systems To minimize effect of genetic confounding and
with enhanced aerenchyma that can provide less increase precision of the analysis, the above root
resistant pathway for internal atmospheric O2 diffu- trait responses were validated using the chromo-
sion to the root tips is a root response to sudden some segment substitution lines (CSSL) of Nippon-
waterlogging (Colmer 2003; Justin and Armstrong bare (japonica) carrying overlapping chromosome
1987; Suralta and Yamauchi 2008). Such ability has segments of Kasalath (indica) (Suralta et al. 2008b).
been defined as phenotypic plasticity (O’Toole and In that study, we identified and selected one line
Bland 1987), which plays key roles in plant (CSSL47) with no significant difference in shoot and
adaptation to various stress conditions (Wang and root growth from Nipponbare under non-stressed
Yamauchi 2006; Yamauchi et al. 1996). (continuously well-aerated) conditions. CSSL47,
Under fluctuating soil moistures, we assumed however, consistently showed more plastic root
that rice plants develop their root system adapted to development than Nipponbare in terms of more
Plant Soil (2010) 332:87–104 89

branching of lateral roots and more aerenchyma Experiment 1: Transient droughted-to-waterlogged

formation under short-duration of transient moisture condition
stresses in hydroponics such as O2-deficient-to-
droughted and vice-versa. Interestingly, root plastic Seeds of Nipponbare and CSSL47 were soaked in
development responses of CSSL47 did not contrib- water and incubated in a seed germinator main-
ute to greater shoot dry matter production. In the tained at 28°C for 24 h prior to sowing. Three pre-
present study, therefore, we attempted to test the germinated seeds from each genotype were grown
hypothesis that the plastic responses in root traits are in a PVC box (25 cm×2 cm ×40 cm, L×W×H)
useful in maintaining crop productivity if plants filled with air-dried alluvial loamy sand following
are grown under prolonged transient moisture the method of Kono et al. (1987a). The soil was pre-
stresses in soils. mixed with fertilizer containing 60 mg nitrogen (N),
The studies presented here examined root plastic 80 mg phosphorus (P), and 70 mg potassium (K).
development through aerenchyma formation and The plants were grown for 36 days. The seedlings
lateral root production, and their functions to were later thinned to one seedling per box at 3 days
maintain atmospheric O2 transport and soil water after sowing (DAS).
uptake under prolonged transient soil moisture
stresses. Such responses were also quantified in Soil moisture treatments and plant sampling
terms of their contribution to the maintenance of
physiological responses such as stomatal conduc- Two soil moisture treatments were done in this
tance, transpiration, and photosynthesis and ulti- experiment: continuously waterlogged (CWL) as
mately, shoot growth in terms of dry matter control; and transient droughted-to-waterlogged
production. To increase precision of the quantitative (D-W) conditions. In CWL, water level was increased
analysis, we used previously selected CSSL47 from and maintained at 2 cm above the soil surface from 3
short-duration transient moisture stresses in hydro- DAS until the end of the experiment (36 DAS). For
ponics and compared with the recurrent parent the D–W condition, the soil in the box was first
Nipponbare to minimize the effect of genetic con- submerged for 24 h and then drained. The soil was
founding. allowed to dry and maintained at 10% soil moisture
content (SMC; −0.17 MPa) from sowing up to 21
DAS. After which, the droughted plants of both
Materials and methods genotypes were subjected to waterlogged conditions
for another 15 days. The initial 10% SMC was close
Plant materials to the critical soil moisture (8% SMC or −0.28 MPa)
when most legumes and cereals we have tested started
The two experiments conducted in this study showing sign of wilting, especially in the late
utilized a selected line CSSL47 drawn from 54 afternoon, but recovered the next morning.
chromosome segment substitution lines (CSSL) of All treatments were watered every 2 days to set the
Nipponbare (japonica type) carrying an overlapping desired SMC. Water was added to replace the water
chromosome segments of Kasalath (indica type) and lost through evapotranspiration and to maintain target
the recurrent parent Nipponbare. The CSSL47 have SMC. For lower SMC, the difference in soil moisture
substituted segments in 8 of 12 chromosomes in between the topmost and bottom portions when the
CSSL47 i.e., chr 3 (between loci R1927 and R1925), soil was allowed to reach 15% SMC after 7 days
chr 4 (between R2373 and C734), chr 6 (between without watering was only 1.3%. At 12% SMC after
loci R2147 and C235), chr 7 (between loci C261 and 14 days without watering, the difference was 0.3%
R565), chr 8 (between loci C1107 and R202), chr 10 (Kono et al. 1987b). Since we observed a 2-day
(between loci C701 and R1629 and loci C488 and watering interval, differences in moisture between top
C223) chr 11 (between loci C447 and C3 and at and bottom soils in the box should have been much
R1506) and chr 12 (between loci G24B and R617) smaller.
(http://www.rgrc.dna.affrc.go.jp/ineNKCSSL54. Plant samplings were done 21 DAS (end of initial
html). drought or waterlogging) and 36 DAS (15 days after
90 Plant Soil (2010) 332:87–104

transient or continuous waterlogging). Three boxes are expressed as percentages of the total respiration
(1 box = 1 replication) from each treatment were measured with the roots excised.
collected from each sampling period.
Root porosity measurements
Physiological measurements
The internal gas space (porosity) may not be identical
Stomatal conductance, transpiration, and photosyn- with aerenchyma. For instance, rice roots have root
thesis of the second-youngest fully-expanded leaf porosity of ∼9% at 20–25 mm behind the root tips
were measured using a portable photosynthesis even with the absence of aerenchyma (Armstrong
system (LI-6400, LI-COR, USA) starting at 1000 h. 1971). This means that the estimates of aerenchyma
Measurements were made every 3 days starting at based on porosity may possibly overestimate its size.
21 DAS (end of initial drought or waterlogging) up However, there is no effective method to distinguish
to 36 DAS (15 days after transient or continuous this aerenchyma from total porosity. Thus, we used
waterlogging). total porosity as an estimate of aerenchyma develop-
ment in this paper.
Root oxygen consumption measurements The coleoptilar nodal root axis was used for root
porosity measurement following the microbalance
Cutting the shoots and sealing the cut portion prevent method of Visser and Bögenmann (2003). Coleoptilar
the entry of atmospheric O2 into the plant’s gas space nodal roots developed a few days after the emergence
system (Teal and Kanwisher 1966), allowing aeren- of seminal root axis and, therefore, are assumed to be
chyma function to be investigated. The difference then exposed to both the initial drought and transient
in flux rates between the cut and sealed root system waterlogging. A 2-cm segment from both the basal
and intact plant system equates to the amount of O2 and apical portions of the roots was cut and excluded
transported internally through the plant (Lee 2003; from the measurements. Briefly, the length of the
Maricle and Lee 2007; Suralta and Yamauchi 2008). remaining root axis was divided equally into three
Intact plants with shoots and roots were carefully parts and designated as basal (B), middle (M) and
sampled from the box to prevent damage to root apical (A) portions. From each portion, five 1-cm
system. The roots were washed to remove soil and segments were further sampled. The five 1-cm seg-
other dirt. Root O2 consumptions were determined by ments from the basal portion were cut starting from
sealing the roots of an intact plant into a flask of the basal proximity. These segments were designated
nitrogen (N2)-flushed water with initial O2 concentra- as B1, B2, B3, B4, and B5.On the other hand, cuttings
tion of 19.0 μmol measured using a dissolved O2 (DO) from the apical portion were done from the apical
meter. After 2 h, subsequent decrease in flask O2 proximity and designated as A5, A4, A3, A2, and A1.
concentration was recorded to assess O2 consumption In the middle portions, five 1-cm segments were
by the roots. Background rates of O2 flux were sampled using the mid 1-cm segment as reference and
likewise determined in flask with N2-flushed water designated as M3. The two 1-cm segments sampled
with the same initial O2 concentration as above but going basally were designated as M2 and M1. The
without suspended plants. A change in O2 concentra- other 2-cm segments sampled going apically were
tion in the blank flask was used to correct O2 designated as M4 and M5. Each 1-cm root segment
consumption readings in flask with suspended plants. was cut with a sharp razor blade and gently blotted by
Shoots were removed by cutting at the stem base rolling it with a small brush on tissue paper for about
and the cut base was sealed with thick parafilm. O2 2 s to remove adherent water. Then, to prevent weight
consumption from the flask was measured again after loss by evaporation, the segments were transferred
2 h to determine the changes in root O2 consumptions into a capsule with cover that had been tared on a
without shoot. Differences in root O2 consumption microbalance. After closing the capsule, the segments
between plants with and without shoot indicate the were weighed (w1 in µg), transferred to a holder with
contribution of aerenchyma to the internal transport of small vials filled with water, and stored for 30 min.
atmospheric O2 to the roots with O2 deficiency. The Up to 36 samples were weighed before they were
increases or decreases in respiratory O2 consumption infiltrated with tap water twice under vacuum for
Plant Soil (2010) 332:87–104 91

30 min each. After water infiltration, the root seg- Experiment 2: Transient waterlogged-to-droughted
ments were blotted again on tissue paper for about 2 s condition
and weighed in a capsule (w2 in µg). Using the
specific weight (SW) obtained from larger samples The same set of genotypes used in Experiment 1
(1.04 g ml−1; Visser and Bögenmann 2003), the was used in this experiment. Pre-germinated seeds
porosity was calculated using the formula: were sown in rootboxes that were prepared as in
Experiment 1.
Porosityð%; v : vÞ ¼ 100  ðw2  w1Þ  SW=w2
Soil moisture treatments and plant sampling
with the specific weight of water being 1.00 g ml−1.
Furthermore, the number of lateral roots from each Four soil moisture treatments were used in this
1-cm segment was also counted and expressed as experiment: continuously waterlogged (CWL) as
linear frequency (the number of lateral roots per unit control; and three transient waterlogged-to-droughted
length root axis; Ito et al. 2006). (W–D) conditions with varying levels of target SMCs.
In CWL, water level was increased and maintained at
Shoot and root development measurements 2 cm above the soil surface from 3 DAS until the end of
the experiment (38 DAS). In W–D, the soil inside the
After O2 consumption and root porosity measure- box was first waterlogged from 3 to 14 DAS. Thereafter,
ments, the main stem leaf number and number of water was drained, allowed to dry and maintained to a
stems of each plant were counted and then cut, oven desired moisture levels. Water levels were 30% SMC
dried at 80°C for 48 h, and weighed. Thereafter, the (−0.003 MPa), 25% SMC (−0.014 MPa) and 20% SMC
root system was stored in FAA (formalin: acetic acid: (−0.040 MPa), hereafter referred to as W–D30, W–D25,
70% ethanol = 1: 1: 18 by volume) solution for and W–D20, respectively. Drought treatments imposed
further measurements. The length of seminal roots through progressive soil drying were terminated at 38
was measured using a ruler and the number of lateral DAS. These drought stress intensities are well within
roots along its axis was counted. The number of nodal the reported range of soil water potentials (from 0
roots was manually counted. For total root length, to −0.05 MPa) that significantly reduce rice yields
each root sample in FAA was rinsed with water and (Bouman and Toung 2001). The decrease in soil
spread on a transparent sheet without overlapping. moisture of each box was monitored every 2 days to
Digitized images were taken using a scanner with a record the amount of evapotranspiration. A few boxes
resolution of 300 dpi and an output format of 256 (n=3) for both the CWL and transient W–D conditions
grey scales. The total root length was determined were not planted and were used to measure the amount
using a macro program developed by Kimura et al. of water lost through evaporation. In this way, the
(1999) and Kimura and Yamasaki (2001) on the NIH amount of water lost by transpiration alone could be
image software version 1.60 (public domain released estimated. Watering was done every 2 days or
by the National Institute of Health, U.S.A.). whenever necessary to maintain the desired SMC.
After scanning, the root samples were oven dried at Samplings were made at 14 DAS (after 14 days of
80°C for 48 h before weighing. The specific root initial waterlogging) and at 38 DAS (after 24 days of
length (SRL) was calculated as root length per unit continuously waterlogged or transient droughted
root dry weight. The variations in SRL can be conditions). Three plants were collected from each
attributed to the differences in production of lateral treatment for each sampling period.
roots (Bañoc et al. 2000b), root density (Eissenstat
1991), or the combination of both. Physiological measurements

Statistical analysis Stomatal conductance, transpiration, and photosyn-

thesis of the second-youngest fully-expanded leaf
The treatments were arranged in split-plot design with were measured using a portable photosynthesis
three replications. Soil moisture treatment was used as system (LI-6400, LI-COR, USA) starting at 1000 h.
mainplot while the genotypes as subplot. Measurements were done at 14 DAS and 38 DAS.
92 Plant Soil (2010) 332:87–104

Shoot and root development measurements Results

The main stem leaf number and number of stems of Experiment 1: Effects of drought followed
each plant were counted, then cut, oven dried at 80°C by waterlogged (D–W) condition
for 48 h before weighing. The whole root system was
sampled thereafter, using a pinboard following the Shoot and root development
methods of Kono et al. (1987a). The extracted root
systems embedded in plastic sheets were stored in Main stem leaf number as well as shoot and root
FAA for further measurements. growth were not significantly different between
For total root length, each root sample was CSSL47 and Nipponbare after initial waterlogging
thoroughly rinsed with water to remove FAA and (from 0 to 21 DAS) (Table 1). The removal of
stained in 0.25% Coomassie Brilliant Blue R 250 shoots from intact plants significantly increased root
aqueous solution for 48 h. This staining procedure O2 consumption from the hypoxic medium in both
was indispensable to take high-resolution digital genotypes (Table 1). The estimated atmospheric O2
photographs of the entire root system including fine contributed by aerenchyma was not significantly
lateral roots. After staining, the root samples were different between the two genotypes (Table 1).
washed gently with running water to remove excess Likewise, the responses of those measured parame-
stains. Thereafter, each root sample was put in a light ters to initial drought were not significantly different
box and photographed using transmitted light. Digi- between the two genotypes (Table 1). Under
tized photographs of the root system profile were drought, the main stem leaf number was not
taken using a Canon digital camera at highest significantly affected in both genotypes (Table 1).
resolution (3,456×2,304 pixels). The digital images Meanwhile, the effects of drought treatment on other
in jpeg format were downloaded in a computer and parameters were significant. Specifically, initial
converted into tiff format for total root length drought significantly reduced the shoot dry weight,
measurements. The total root length was measured number of stems per plant, total root length, number
using a macro program on NIH developed by Kimura of nodal roots, and specific root length (SRL), as
et al. (1999) and Kimura and Yamasaki (2001). compared with their waterlogged controls (Table 1).
The number of nodal roots was manually counted. In contrast, initial drought significantly promoted the
From each plant, two nodal roots were sampled (one length of seminal roots (Table 1). Furthermore, the
each from first and sixth internodes). Each nodal root removal of shoots from intact plants of initially
was cut into 4-cm segments keeping the lateral roots droughted treatments did not significantly increase
intact. In this way, the number of each type of lateral root O2 consumption from the hypoxic medium in
root was determined. The lateral roots were classified both genotypes (Table 1). As a result, the atmo-
into L and S types that have been shown to differ in spheric O2 contributed by aerenchyma was signifi-
anatomy, morphology, developmental characteristics, cantly lower in both genotypes, compared with their
carbon and nitrogen dynamics (Yamauchi et al. 1996) controls (Table 1).
and the genetic control of development (Wang et al. Under CWL condition for 36 days, the main
2005). The lateral roots that branched into higher stem leaf number was not significantly different
order laterals were regarded as L type and the non- between CSSL47 and Nipponbare (Table 2). Like-
branching roots as S type. Each type of lateral root wise, shoot and root development, and other mea-
was expressed as linear frequency (the number of sured parameters were not significantly different
lateral roots per unit length of root axis; Ito et al. between the two genotypes (Table 2). The removal
2006). of shoots from an intact plant significantly in-
creased O2 consumptions from the hypoxic medium
Statistical analysis (Table 2). The estimated atmospheric O2 contributed
by aerenchyma, however, was not significantly
The treatments were arranged in split-plot design with different between the two genotypes (Table 2).
three replications. The soil moisture treatments were Under drought followed by waterlogged (D–W)
used as mainplot while the genotypes as subplot. condition for 15 days, the main stem leaf number
Table 1 Shoot and root growth, specific root length and atmospheric O2 contributed by aerenchyma in Nipponbare and CSSL47 after 21 days of waterlogged or droughted soil
conditions. Values are means of 3 replicates

Soil moisture condition/ Main stem SDW Stem NR TRL Seminal SRL Root O2 consumptions O2 contribution
Genotypes leaf number (mg plant−1) (no. plant−1) (no. plant−1) (cm plant−1) RL (cm) (m RL g−1 RDW) (umol g−1 RDW h−1) through RP (%)a

With shoot Without shoot

Waterlogged
Nipponbare 5.2 a 395.0 a 3.0 a 41.0 a 2,788.0 a 22.3 b 474.4 a −11.2 a −16.6 a * 32.7 a
Plant Soil (2010) 332:87–104

CSSL47 5.1 a 429.0 a 3.0 a 48.7 a 3,229.0 a 19.3 b 485.5 a −9.2 a −14.4 a * 36.5 a
Droughted
ns
Nipponbare 4.9 a 97.0 b 1.0 b 3.3 b 706.7 b 39.8 a 360.0 b −10.2 a −10.6 b 3.6 b
ns
CSSL47 4.9 a 107.0 b 1.0 b 3.0 b 707.9 b 30.0 a 368.9 b −10.6 a −10.8 b 2.3 b

SDW shoot dry weight; RL root length; TRL total root length; NR nodal root; SRL specific root length; RDW root dry weight; RP root porosity
a
The increases or decreases in respiratory O2 consumption are expressed as percentages of the total respiration measured with the roots excised
In a column, means followed by the same letters are not significantly different at LSD0.05
ns not significant
*significant at P<0.05 between root O2 consumptions of plants with and without shoot

Table 2 Shoot and root growth, specific root length and O2 contributed by aerenchyma in Nipponbare and CSSL47 after 36 days of continuous waterlogging (CWL) or transient
droughted for 21 days followed by waterlogging for 15 days (D–W). Values are means of 3 replicates

Soil moisture condition/ Main stem SDW Stem NR TRL Seminal SRL Root O2 consumptions O2 contribution
Genotypes leaf number (mg plant−1) (no. plant−1) (no. plant−1) (cm plant−1) RL (cm) (m RL g−1 RDW) (umol g−1 RDW h−1) through RP (%)a

With shoot Without shoot

CWL
Nipponbare 8.6 a 2,440.0 a 5.7 a 162.7 a 18,254.7 a 21.7 c 350.5 b −10.9 b −18.5 a * 40.5 a
CSSL47 8.8 a 2,460.0 a 5.0 a 170.0 a 19,259.0 a 20.8 c 340.3 b −11.0 b −18.4 a * 40.4 a
D–W
Nipponbare 8.5 a 810.0 c 3.0 b 62.0 c 5,124.0 c 30.7 b 345.8 b −12.9 a −18.9 a * 32.1 b
CSSL47 8.4 a 1,033.0 b 3.0 b 84.0 b 7,537.0 b 34.0 a 450.3 a −11.8 b −19.2 a * 38.5 a

SDW shoot dry weight; RL root length; TRL total root length; NR nodal root; SRL specific root length; RDW root dry weight; RP root porosity
a
The increases or decreases in respiratory O2 consumption are expressed as percentages of the total respiration measured with the roots excised
In a column, means followed by the same letters are not significantly different at LSD0.05
*significant at P<0.05 between root O2 consumptions of plants with and without shoot
93
94 Plant Soil (2010) 332:87–104

was not significantly different between the two Linear frequency of lateral roots along the coleoptilar
genotypes (Table 2). However, W–D significantly nodal root axis
reduced the shoot dry weight, total root length and
number of nodal roots in both genotypes, but the The mean linear frequency of lateral roots on seg-
reduction was significantly less in CSSL47 than in ments along the coleoptilar nodal root axis was
Nipponbare (Table 2). The number of stems per significantly reduced by D–W condition in Nippon-
plant was also significantly reduced at almost bare but it was not affected in CSSL47 (Fig. 3). Such
similar rates for both genotypes (Table 2). More- reduction in Nipponbare was attributed to the signif-
over, the length of seminal root was significantly icant decreases in linear frequency of lateral roots
promoted in both genotypes, but the promotion particularly on segments along the basal and apical
was much greater in CSSL47 than in Nipponbare portions of the coleoptilar nodal root axis (Fig. 3). In
(Table 2). contrast, the linear frequency of lateral roots on
SRL was not significantly affected by D–W segments all throughout the coleoptilar nodal root
condition in Nipponbare while in CSSL47 it was axis of CSSL47 was not significantly affected by
significantly increased (Table 2). Furthermore, the transient D–W condition.
removal of shoots from an intact plant from W–D
treatments also significantly increased O2 consump- Experiment 2: Waterlogged followed by droughted
tion from the hypoxic medium in both genotypes (W–D) condition
(Table 2). However, for Nipponbare, the estimated
atmospheric O2 contributed by aerenchyma under this Main stem leaf number, shoot and root growth,
condition was significantly lower than under contin- number of stems per plant, stomatal conductance,
uous flooding (Table 2). transpiration, and photosynthesis were not signifi-
cantly different between CSSL47 and Nipponbare
Stomatal conductance, transpiration, after initial waterlogging (14 DAS; Table 3).
and photosynthesis
Shoot and root growth
At the end of initial drought (21 DAS), stomatal
conductance, transpiration, and photosynthesis were The main stem leaf number was not significantly
significantly reduced in both genotypes (Fig. 1). different between the two genotypes at any of the soil
During transient waterlogging period (22 to 36 DAS) moisture treatments (Table 4). Shoot dry weights under
under D–W condition, CSSL47 recovered its CWL and W–D30 (waterlogging followed by drought
stomatal conductance, transpiration, and photosyn- to 30% SMC) conditions were not significantly
thesis back to the level of its control after 12 days different between CSSL47 and Nipponbare (Table 4).
of waterlogging. In contrast, Nipponbare only At W–D25 and W–D20 however, shoot dry weight was
showed partial recovery of stomatal conductance, significantly greater in CSSL47 than in Nipponbare
transpiration, and photosynthesis during transient (Table 4). The number of stems per plant was not
waterlogging (Fig. 1). significantly different between the two genotypes at
any of the soil moisture treatments (Table 4).
Root porosity in segments along the coleoptilar nodal The root system profiles of CSSL47 and Nippon-
root axis bare grown under CWL and W–D conditions are
shown in Fig. 4. Under CWL, the root system
Compared with their CWL controls, mean root development was comparable between the two geno-
porosity under D–W condition was significantly types. At W–D30, the root system developments of
lower in Nipponbare while it was not affected in both genotypes appeared to be slightly inhibited at
CSSL47 (Fig. 2). The lower mean root porosity in almost the same rates, compared with their water-
Nipponbare was particularly attributed to the signif- logged controls. At W–D25 and W–D20 however, the
icantly lower root porosities in segments at the basal root system developments of both genotypes were
and middle portions of the coleoptilar nodal root axis evidently inhibited (i.e. nodal root productions) with
(Fig. 2). Nipponbare exhibiting greater inhibitions than CSSL47
Plant Soil (2010) 332:87–104 95

Fig. 1 Stomatal conductance, transpiration, and photosynthesis Data are means of 3 replicates. Significance between the two
of CSSL47 and Nipponbare grown either under 36 days of treatments at each time point: ns not significant; *, **,
continuous waterlogging (CWL, ■), or after 21 days of initial significant at P<0.05 and 0.01, respectively
drought (day 0) followed by 15 days of waterlogging (D–W, □).

(Fig. 4). The quantitative data for different root frequency of L type lateral roots was significantly
components of these root system profiles are shown greater in CSSL47 than in Nipponbare (Table 5). In
in Tables 4 and 5. Under CWL and W–D30 conditions, contrast, the linear frequency of S type lateral roots of
the number of nodal roots per plant, total nodal root the two genotypes was not significantly different at
length (Table 4), and total root length of CSSL47 any of the soil moisture treatments (Table 5).
(Table 5) were not significantly different from
Nipponbare. At W–D25 and W–D20 however, the Stomatal conductance, transpiration,
above root traits were significantly greater in CSSL47 and photosynthesis
than in Nipponbare (Tables 4 and 5).
The number of L type lateral roots on the nodal Stomatal conductance, transpiration, and photosyn-
root axis of the two genotypes was not significantly thesis were not significantly different between the two
different under CWL and W–D30 conditions (Table 5). genotypes under CWL and W–D 30 conditions
At W–D25 and W–D20 conditions, however, the linear (Fig. 5). At W–D25, CSSL47 had significantly higher
96 Plant Soil (2010) 332:87–104

Regression analysis showed shoot dry matter

production was significantly influenced by WU but
not by WUE (Fig. 6). The variation in WU contrib-
uted to 67% of the variation in shoot dry matter
production during the droughted period in W–D
conditions (Fig. 6).
The water uptake rate, which ranged from 50 to
60 mg H2O cm−1 root length, was not significantly
different between the two genotypes at any of the soil
moisture treatments (data not shown).

Discussion

This study showed that CSSL47 did not significantly

differ from Nipponbare in developmental age of their
seedlings as indicated by main stem leaf number

Fig. 2 Root porosity in segments along the coleoptilar nodal root

axes of CSSL47 and Nipponbare grown either under 36 days of
continuous waterlogging (CWL, ■) or transient droughted for
21 days followed by waterlogging for 15 days (D–W, □). Root
segments were from the basal (B), middle (M), and apical (A)
portion of the root axis. Data are means of 3 replications. The insert
showed the mean root porosity for all segments. Significance
between the two treatments within each segment: ns not significant;
*, **, significant at P<0.05 and 0.01, respectively

transpiration and photosynthesis, but similar stoma-

tal conductance to that of Nipponbare (Fig. 5). At
W–D20, stomatal conductance, transpiration, and
photosynthesis were all significantly higher in CSSL47
than in Nipponbare (Fig. 5).

Water use, water use efficiency, and water uptake rate

Water use (WU) or the whole plant transpiration

was calculated between 15 to 38 DAS when the
plants were either continuously waterlogged or
subjected to droughted conditions after initial
Fig. 3 Linear frequency of lateral roots in segments along the
waterlogging. WU was not significantly different
coleoptilar nodal root axes of CSSL47 and Nipponbare grown
between the two genotypes under CWL and W–D30 either under 36 days of continuous waterlogging (CWL, ■) or
conditions (Table 6). At W–D25 and W–D20 con- transient droughted for 21 days followed by waterlogging for
ditions, WU of CSSL47 was significantly higher 15 days (D–W, □). Root segments were from the basal (B), middle
(M), and apical (A) portion of the root axis. Data are means of 3
than that of Nipponbare (Table 6). In contrast, WUE
replications. The insert showed the mean number of lateral roots
did not significantly differ between the two geno- for all segments. Significance between the two treatments in each
types at any of the soil moisture treatments (Table 6). segment: ns not significant; *, significant at P<0.05
Table 3 Shoot and root growth, stomatal conductance, transpiration, and photosynthesis of Nipponbare and CSSL47 under 14 days of initial waterlogged soil condition. Values are
means of 3 replicates

Genotype Main stem SDW Stem NR TRL Stomatal conductance Transpiration Photosynthesis
leaf number (mg plant−1) (no. plant−1) (no. plant−1) (cm plant−1) (mol m−2 s−1) (mmol m−2 s−1) (μmol m−2 s−1)

Nipponbare 4.2 50.0 1.0 16.1 535.2 0.9 12.0 26.0

CSSL47 4.1 ns 50.0 ns 1.0 ns 15.9 ns 547.2 ns 1.0 ns 11.0 ns 27.0 ns
Plant Soil (2010) 332:87–104

SDW shoot dry weight; NR nodal root; TRL total root length
ns not significantly different from Nipponbare

Table 4 Shoot and root growth of Nipponbare and CSSL47 grown either under 38 days of continuous waterlogging (CWL) or transient waterlogged for 14 days followed by
progressive drought for 24 days (W–D). Values in W–D treatments denote the target soil moisture content (%) maintained after progressive soil drying

Soil moisture conditions Main stem leaf number Shoot dry weight (mg plant−1) Stem (no. plant−1) Nodal roots (no. plant−1) Total nodal root length (cm)

Nipponbare CSSL47 Nipponbare CSSL47 Nipponbare CSSL47 Nipponbare CSSL47 Nipponbare CSSL47

CWL 9.8 9.5 ns 2,305.7 2,390.0 ns 3.8 4.0 ns 110.7 118.0 ns 2,230.2 2,130.7 ns
W–D30 9.8 9.9 ns 1,776.9 1,844.5 ns 3.4 3.0 ns 78.0 87.0 ns 1,599.2 1,701.0 ns
W–D25 9.7 9.5 ns 1,485.8 2,004.5 ** 3.3 3.3 ns 58.0 97.3 ** 1,172.8 1,744.2 **
W–D20 9.5 9.7 ns 1,644.7 2,090.3 ** 3.3 3.7 ns 60.0 87.0 * 1,079.9 1,475.8 *

ns not significant
*, ** significant at P<0.05 and P<0.01, respectively, between the two genotypes within each moisture treatment level
97
98 Plant Soil (2010) 332:87–104

Fig. 4 Root system profiles of CSSL47 (a–d) and Nipponbare contents. The intact root system was extracted from rootbox
(e–h) grown either under 38 days of continuous waterlogging using a pinboard as described by Kono et al. (1987a). Prior to
(CWL; a, e) or transient waterlogged for 14 days followed by taking digitized photographs set up in a lightbox, these root
progressive drought for 24 days (W–D) at 30% (W–D30; b, f), systems were stained with 0.25% of Coomassie Brilliant Blue
25% (W–D25; c, g) and 20% (W–D20; d, h) target soil moisture R solution for 2 h. Bars=5 cm

Table 5 Total
Total root
root length
lengthand
andlinear
linearfrequency
frequencyofoflateral
lateralroots
roots
on thewaterlogged
nodal root axis
for of
14Nipponbare
days followed
and CSSL47
by progressive
grown either
drought
under
for
38 days
on the nodal
of continuous
root axis waterlogging
of Nipponbare(CWL)
and CSSL47
or transient
grownwaterlogged
either 24
for days
14 days
(W–D).
followed
Values
by in
progressive
W–D treatments
droughtdenote
for 24the
days
target
(W–D).
soil
Values 38
under in W–D
days oftreatments
continuous
denote
waterlogging
the target (CWL)
soil moisture
or transient
content (%)moisture
maintained
content
after
(%)
progressive
maintainedsoil
after
drying
progressive soil drying

Soil moisture conditions Total root length (cm) Linear frequency Linear frequency
(L-type LR cm−1 NR) (S-type LR cm−1 NR)

Nipponbare CSSL47 Nipponbare CSSL47 Nipponbare CSSL47

CWL 13,352.0 12,314.0 ns 0.1 0.1 ns 11.4 10.9 ns

W–D30 11,691.0 11,434.0 ns 1.1 1.3 ns 10.6 10.8 ns
W–D25 10,221.0 12,252.0 ** 1.3 2.5 ** 9.8 10.0 ns
W–D20 9,495.0 11,650.0 * 1.3 1.9 ** 9.6 10.8 ns

LR lateral roots; NR nodal roots

ns not significant
*, ** significant at P<0.05 and P<0.01, respectively, between the two genotypes within each moisture treatment level
Plant Soil (2010) 332:87–104 99

Table 6 Water use (WU) and water use efficiency (WUE) of

Nipponbare and CSSL47 grown either under 38 days of
continuous waterlogging (CWL) or transient waterlogged for
14 days followed by progressive drought for 24 days (W–D).
Values in W–D treatments denote the target soil moisture
content (%) maintained after progressive soil drying

Soil moisture WU WUE

conditions (g plant−1) (mg SDW g−1 H2O)

Nipponbare CSSL47 Nipponbare CSSL47

CWL 684.0 726.0 ns 3.4 3.3 ns

W–D30 669.0 611.0 ns 2.7 3.0 ns
W–D25 469.0 634.0 ** 3.2 3.2 ns
W–D20 470.0 585.0 * 3.5 3.6 ns

SDW shoot dry weight

ns not significant
*, ** significant at P<0.05 and 0.01, respectively, between the
two genotypes within each moisture treatment level

Fig. 5 Stomatal conductance, transpiration, and photosynthesis

of Nipponbare (□) and CSSL47 (■)grown either under 38 days
of continuous waterlogging (CWL) or transient waterlogged for
14 days followed by progressive drought for 24 days (W–D).
Values in W–D treatments denote the target soil moisture
content (%) maintained after progressive soil drying. Signifi-
cance between the two genotypes under each soil moisture
treatment: ns not significant; *, **, significant at P<0.05 and
0.01, respectively

(Tables 2 and 4). Likewise, these two genotypes did

not significantly differ in constitutive shoot and root
system development under continuously waterlogged
conditions (Tables 2, 4 and 5). Thus, it was possible
Fig. 6 Relationship of water use and water use efficiency with
to compare and evaluate the contribution of plastic shoot dry matter production of CSSL47 (■) and Nipponbare (□)
root development that was triggered by transient soil during 15–38 DAS. ns not significant; ** significant at P<0.01
100 Plant Soil (2010) 332:87–104

moisture stresses and their effects on physiological CSSL47 was significantly higher than that of
responses such as stomatal conductance, transpiration, Nipponbare under D–W condition. An increase in
and photosynthesis and ultimately, shoot dry matter SRL is a common response to limitations in nutrient
production with minimal effects of genetic confound- (Schippers and Olff 2000) and water (Bañoc et al.
ing. Furthermore, the shoot and root development were 2000a; Tjoelker et al. 2005). The greater SRL found
not significantly different between the two genotypes in CSSL47 than in Nipponbare under transient D–W
under the initial drought of D–W treatment (Table 1), condition may reflect promoted branching into lateral
and initial waterlogged conditions (Tables 1 and 3). roots and/or enhanced aerenchyma formation under
These facts further indicate that better growth in waterlogged condition, which was related to the
CSSL47 than Nipponbare under both transient soil increase in root porosity (Eissenstat 1991; Raumet et
moisture stresses can be attributed to more promoted al. 2006). As such, droughted roots of CSSL47
root development of CSSL47 than Nipponbare in subjected to sudden waterlogging exhibited faster
response to the second transient stress, which possibly growth for fast and efficient acquisition of resources
was influenced by the preceding moisture stress such as nutrients, to cope up with its overall growth.
(initially droughted or waterlogged conditions). Then, Increased root porosity due to the formation of
such plastic root development in CSSL47 in turn is aerenchyma is one of the most common adaptive
attributable to either one or combinations of the responses of plants such as rice to O2 deficiency (Colmer
substituted segments from Kasalath inserted into 2003; Jackson and Armstrong 1999; Vartapetian and
Nipponbare genetic background found in this line. Jackson 1997; Wang and Yamauchi 2006). Thus, the
Some of the QTL markers contained in the substituted general belief is that waterlogging cannot be stressful
segments in CSSL47 coincided with the QTLs for rice. In this study, however, it is interesting to note
reportedly detected in other mapping populations such that waterlogging is also stressful to rice especially
as root-to-shoot ratio, maximum root length, and root when this stress is preceded by drought. This was
thickness at the base and below 90-cm soil depth clearly shown in Nipponbare in which the ability to
(Champoux et al. 1995; Price et al. 2002; MacMillan et increase root porosity under sudden waterlogged con-
al. 2006). However, none of the marker-linked QTLs ditions was lost when roots were previously exposed to
controlling lateral root production identified in other drought (Fig. 2). On the other hand, CSSL47 was able
mapping populations (i.e. Horii et al. 2006; Zheng et to increase its root porosity under sudden waterlogged
al. 2003) coincided with any of the markers contained conditions even when its roots were previously exposed
in the substituted segments of CSSL47. to drought (Fig. 2). Such increase in root porosity in
CSSL47 facilitated higher efficiency of its root system
Droughted followed by waterlogged (D–W) condition for internal diffusion of atmospheric O2 to the root tips
under transient waterlogging (Table 2). The above
Under D–W condition, although both genotypes were conditions may in part, explain the higher ability for
in similar developmental age of their seedlings based seminal root elongation of CSSL47 than Nipponbare
on main stem leaf number, CSSL47 produced (Table 2) and more branching of lateral roots on the
significantly greater shoot dry matter production than coleoptilar nodal root axis (Fig. 3), which were exposed
Nipponbare (Table 2). This was attributed to more both to initially droughted and transient waterlogged
rapid recovery of stomatal conductance, transpiration, conditions. Furthermore, the ability of CSSL47’s
and photosynthesis in CSSL47 than in Nipponbare droughted roots to continuously grow when subjected
when their droughted plants were subjected to sudden to transient waterlogging may also explain its higher
waterlogged condition (Fig. 1). Rapid recovery in SRL than Nipponbare under D–W condition (Table 2).
stomatal conductance, transpiration, and photosynthe- Such ability is indispensable as it contributed to the
sis under transient D–W conditions in CSSL47 increase in shoot dry matter production (Table 2) via
(Fig. 1) was due to its faster root system development rapid recoveries in stomatal conductance, transpiration,
and recovery than Nipponbare during the transient and photosynthesis (Fig. 1). The increased shoot growth
waterlogged period (Table 2). It was also noted that in turn, provided materials for production and elonga-
SRL of CSSL47 and Nipponbare was similar under tion of new nodal roots (Table 2). The ability to
CWL conditions (Table 2). In contrast, SRL of produce more number of nodal roots, coupled with
Plant Soil (2010) 332:87–104 101

faster elongation, translates to the development of more followed by drought and rewatering. Such trait in
lateral roots. Since lateral roots comprise the greater root plasticity resulted in increased root surface area
portion of the total length of the whole root system which subsequently increased soil water extractions
(Wang et al. 2009; Yamauchi et al. 1987), their (Kamoshita et al. 2000, 2004; Siopongco et al. 2005,
response to moisture stress directly determines total 2006). The greater ability for root growth expressed
root system development. Under O2 deficiency, the in CSSL47 than in Nipponbare under progressive
lateral roots serve as effective sites for radial oxygen drought, contributed to its higher WU (Table 6),
loss, an essential process for detoxifying phytotoxins which resulted in the maintenance of stomatal
and oxidizing reduced nutrient element to maintain conductance, transpiration, and photosynthesis
the viability of roots for efficient nutrient and water (Fig. 5). This ultimately led to a higher shoot dry
uptake (Armstrong and Armstrong 2005; Revsbech matter production in CSSL47 than in Nipponbare
et al. 1999). This eventually support higher shoot dry (Table 4).
matter production.
CSSL47 is unique under transient soil moisture
Waterlogged followed by droughted (W–D) stresses
conditions
Shoot and root system development of CSSL47 is
Under W–D condition, both genotypes were in comparable with Nipponbare under constant
similar developmental age of their seedlings based droughted condition (Table 1). This indicates that
on main stem leaf number in any of the soil moisture they may have similar genetic control for root
treatments (Table 4). However, CSSL47 showed responses to drought. This is consistent with that of
higher shoot dry matter production than Nipponbare Kanou et al. (2007) who showed that CSSL47 did
especially at W–D25 and W–D20 (Table 4). Such not exhibit higher root growth than Nipponbare
greater dry matter production was attributed to the under constant drought. CSSL47 also showed com-
higher ability of CSSL47 than Nipponbare to main- parable shoot and root growth with Nipponbare
tain stomatal conductance, transpiration, and photo- under constant waterlogging (Tables 1, 2, 3, 4 and
synthesis under progressive droughted conditions 5), which was consistent with the result from our
(Fig. 5). earlier shorter-duration hydroponics experiment
Dry matter production, especially under water- (Suralta et al. 2008b). This indicates that plastic
limited condition, is determined by WU and WUE root system development of CSSL47 was a unique
(Kobata et al. 1996) of the plant. In this study, dry response to transient soil moisture stress condi-
matter production under progressive drought in W–D tions. The root system adaptation of CSSL47 to
condition was closely related to WU but not to WUE subsequent moisture stress was not affected by the
(Fig. 6). This indicates that adaptation of rice under preceding contrasting moisture stress, which is
water-limited conditions in terms of growth and different from that of Nipponbare. Field studies
productivity could be achieved mainly through dehy- also confirmed that CSSL47 produced a signifi-
dration avoidance by maintaining water uptake rather cantly higher yield than Nipponbare under inter-
than by tolerance to desiccation, as pointed out by mittent irrigations where there was alternate
Blum (2005), which was accomplished by maintaining recurrence of O 2 deficiency and progressive
higher root growth under water-limited soil conditions. drought. The two genotypes, however, produced
Apparently, CSSL47 had greater ability to main- the same yield under continuously waterlogged
tain root elongation compared to Nipponbare under conditions (Niones et al. 2009; Suralta et al. 2007).
W–D25 and W–D20, due to its higher ability to These findings clearly show that CSSL47 is better
maintain total nodal root production and plastic adapted to the cycle of drought and waterlogging
lateral root production, especially the L type lateral stresses in the field.
roots (Table 5). Our result agrees with that of Bañoc Detailed analyses, however, on plastic root devel-
et al. (2000b), which showed that plasticity in lateral opmental responses especially from the upper nodes
root production, particularly the L type, plays a key to different timing of transient water stresses (i.e.
role in rice adaptation to waterlogged conditions progressive drought and sudden waterlogging) at
102 Plant Soil (2010) 332:87–104

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