Root morphology, hydraulic conductivity and plant water relations of high-yielding rice grown under aerobic conditions

doi:10.1093/aob/mcr184

Ann Bot. 2011 September; 108(3): 575–583.

Published online 2011 August 1. doi: 10.1093/aob/mcr184

PMCID: PMC3158697

Root morphology, hydraulic conductivity and plant water relations of high-yielding rice grown under aerobic conditions

Yoichiro Kato^* and Midori Okami

Institute for Sustainable Agro-ecosystem Services, The University of Tokyo, Tokyo 188-0002, Japan

^*For correspondence. E-mail agrkato/at/mail.ecc.u-tokyo.ac.jp

Received April 6, 2011; Revisions requested May 10, 2011; Accepted May 23, 2011.

Abstract

Background and Aims

Increasing physical water scarcity is a major constraint for irrigated rice (Oryza sativa) production. ‘Aerobic rice culture’ aims to maximize yield per unit water input by growing plants in aerobic soil without flooding or puddling. The objective was to determine (a) the effect of water management on root morphology and hydraulic conductance, and (b) their roles in plant–water relationships and stomatal conductance in aerobic culture.

Methods

Root system development, stomatal conductance (g_s) and leaf water potential (Ψ_leaf) were monitored in a high-yielding rice cultivar (‘Takanari’) under flooded and aerobic conditions at two soil moisture levels [nearly saturated (> –10 kPa) and mildly dry (> –30 kPa)] over 2 years. In an ancillary pot experiment, whole-plant hydraulic conductivity (soil-leaf hydraulic conductance; K_pa) was measured under flooded and aerobic conditions.

Key Results

Adventitious root emergence and lateral root proliferation were restricted even under nearly saturated conditions, resulting in a 72–85 % reduction in total root length under aerobic culture conditions. Because of their reduced rooting size, plants grown under aerobic conditions tended to have lower K_pa than plants grown under flooded conditions. Ψ_leaf was always significantly lower in aerobic culture than in flooded culture, while g_s was unchanged when the soil moisture was at around field capacity. g_s was inevitably reduced when the soil water potential at 20-cm depth reached –20 kPa.

Conclusions

Unstable performance of rice in water-saving cultivations is often associated with reduction in Ψ_leaf. Ψ_leaf may reduce even if K_pa is not significantly changed, but the lower Ψ_leaf would certainly occur in case K_pa reduces as a result of lower water-uptake capacity under aerobic conditions. Rice performance in aerobic culture might be improved through genetic manipulation that promotes lateral root branching and rhizogenesis as well as deep rooting.

Keywords: Aerobic rice, leaf water potential, Oryza sativa, root system architecture, stomatal conductance, water-saving technology

INTRODUCTION

Plants have a variety of successful strategic adaptations to harsh environments. After germination, they cannot escape local conditions and adaptation is essential for survival. Adjustment of water uptake to soil-water availability through modifications in physiology, and morphology and anatomy of roots is particularly crucial. For example, desert succulents are able to survive prolonged drought by stopping hydraulic water flow through large accumulations of suberin in the exodermal and endodermal cells; this mechanism permits gradual exploitation of residual soil moisture (North and Nobel, 1998). Under severe drought, these plants also down-regulate water transport activity across the cell membrane, a process mediated by aquaporin function (Maurel et al., 2010), and lateral root emergence ceases (North and Nobel, 2000). Reliance on main rather than ephemeral lateral roots for water uptake is less costly under arid conditions.

Agriculturists have pursued better crop adaptations to soil water deficits in systems that depend on rain-fed water inputs; under these circumstances, crop water uptake ability plays a pivotal role in crop yield (Boyer, 1982). Across the soil–plant–atmosphere continuum, hydraulic water flow is induced by the gradient between soil water potential (Ψ_soil) and leaf water potential (Ψ_leaf). Plant water uptake is determined by Ψ_soil, Ψ_leaf and the hydraulic conductance of water transport from roots to leaves (whole-plant hydraulic conductivity, K_pa; Boyer, 1996). K_pa in intensely transpiring plants is largely determined by hydraulic conductance of the root system, which can be used to estimate water uptake ability of roots (Boyer, 1969; Hirasawa and Ishihara, 1991; Steudle and Peterson, 1998). Consequently, numerous studies have determined responses of crops to soil drying through measurements of root-system hydraulic conductance normalized by root length or root surface area (root hydraulic conductivity, L_p; Steudle, 2000).

Agriculture consumes 70 % of the fresh water resource, but less water is becoming available for irrigation owing to the global climate change and competition from urbanization and industrial development (Pennisi, 2008). In particular, increasing physical water scarcity is a main constraint for irrigated rice (Oryza sativa) production (Peng et al., 2009). To cope with water shortage, water-saving rice cultivation technologies are being developed (Bouman et al., 2007). ‘Aerobic rice culture’ is an emerging cultivation system that aims to maximize crop water productivity (yield/water input) by growing plants in aerobic soil without flooding or puddling (Matsunami et al., 2009; Matsuo and Mochizuki, 2009). The procedure may reduce irrigation water consumption to less than half that required for conventional flooded culture, but aerobic culture often causes a significant yield loss (Peng et al., 2006). As in the development of ‘deficit irrigation’ technology in vineyards for safe reduction of agricultural water use (Chaves et al., 2010), interpreting plant physiological responses to soil moisture regimens is vital for determining appropriate irrigation schemes in aerobic rice culture. This knowledge will also facilitate genetic improvement of rice for water-saving cultivations.

Rice has many traits derived from its semi-aquatic ancestor (e.g. shallow root system), but at the same time it has an ability to adapt to soil water deficit (Gowda et al., 2011). A sensitive stomatal closure response to soil water deficit efficiently conserves plant internal water (Parent et al., 2010). Maintaining elevated L_p and promptly elongating lateral roots when soil dries are also drought resistance mechanisms (Matsuo et al., 2009; Kano et al., 2011). Some drought-adaptive traits would probably be effective for minimizing yield loss in aerobic culture, but there is limited knowledge on water uptake and plant water relations in this newly developed water-saving technology. Particularly, root growth and water uptake ability by the roots are expected to have vital roles in plant water relations (Lafitte and Bennett, 2002). Previous studies have postulated that rice root growth may be severely restricted in water-saving aerobic culture (in comparison to conventional flooded culture) (Kato and Okami, 2010; Kato et al., 2010). Since size of the root system is the primary determinant of K_pa in field crops (Jiang et al., 1988; Adachi et al., 2010, 2011), soil water management may affect transpiration rate and/or plant water relations largely through modifying root system development.

The objective of this study was to determine transpiration rate, stomatal conductance (g_s) and plant water relations in high-yielding rice grown under water-saving aerobic culture; comparisons were made with plant performance under conventional flooded culture. Specifically, our hypothesis is that rice is poorly adapted to aerobic culture because of limited root system development under aerobic conditions. We discuss the mechanism underlying effects of water management on plant water relations from the perspective of water uptake capacity (root length) and water uptake ability (hydraulic conductance).

MATERIALS AND METHODS

Set-up of field trials

Experiments were conducted at the Institute for Sustainable Agro-ecosystem Services, The University of Tokyo, Tokyo, Japan (35°43′N, 139°32′E) during the summers (May to October) of 2008 and 2009. The soil at the site is a volcanic ash type (Typic Melanudand according to USDA Soil Taxonomy; sand 51 %, silt 34 %, clay 15 %). Weather data were obtained from Tokyo meteorological stations (20 km from the sites): mean air temperatures from May to October were 23·1 °C in 2008 and 23·0 °C in 2009 (Table 1). Rice plants were grown in lowland fields under three types of water management, i.e. aerobic, near-saturated and flooded. Fields had been uniformly managed for conventional flooded rice culture for >10 years before experiments began, thus treatments were arranged in a completely randomized design with three replicates for each. The plots used for treatments (20 m²) were separated by 1-m bunds. Plastic boards were inserted to 50-cm depth into the soil to prevent lateral water movement above rooting depth between fields. Fields for aerobic and near-saturated soil treatments were not puddled. Flush irrigation was provided in 2008 and sprinkler irrigation in 2009 to aerobic and saturated treatments. Aerobic treatment occasionally received irrigation when Ψ_soil at 20-cm depth reached approx. –30 kPa; it is the standard irrigation scheme of aerobic rice culture (Peng et al., 2006). On the other hand, saturated treatment received 10–15 mm of irrigation daily to avoid dry soil conditions (below field capacity). Total water inputs (irrigation plus rainfall) were approx. 1500 mm and 2500 mm in aerobic and saturated treatments, respectively. Total water input to flooded soil was not measured, but it is normally in the range of 3000–3500 mm at the site (Kato et al., 2009). Fields were puddled in the flooded treatment, and a 5–10 cm water depth was maintained continually after seedling establishment. An indica rice cultivar, ‘Takanari’, which is one of the highest-yielding cultivars available in Japan (Takai et al., 2006) was planted. Four or five seeds were directly sown in each hill on 12 May in 2008 and 18 May in 2009. Plants were thinned to one per hill after seedling establishment. Hill spacing was 25 × 25 cm in 2008 and 20 × 20 cm in 2009. Chemical fertilizer (N, P, K = 60, 39, 67 kg ha⁻¹) was applied before sowing, and (NH₄)₂SO₄ was top-dressed at 2- to 4-wk intervals (total N = 240 kg ha⁻¹ in 2008 and 160 kg ha⁻¹ in 2009).

Table 1.

Monthly means for daily air temperature, daily solar radiation and total rainfall in the summer season

Set-up of pot experiment

Rice plants (‘Takanari’) were grown under three water regimens (one flooded and two aerobic conditions) in pots (26 cm diameter, 30 cm depth) in a naturally lit greenhouse in 2010. Plots with different water regimens were arranged in a randomized complete block design with five replicates. Each plot contained two pots, i.e. plot size was 1·3 m⁻². Pots were adequately isolated (1·5 pots m⁻²). Mean temperature and humidity were 25·6 °C and 70·0 %, respectively. Pots in the flooded treatment were filled with puddled soil from lowland fields, while pots in the aerobic treatments were filled with non-puddled soil from upland fields, both at a bulk density of approx. 0·75 g cm⁻³ (12-L of soil). To ensure uniform seedling establishment, two 8-d-old seedlings (raised in the nursery trays) were transplanted to the centre of each pot on 22 May 2010. Chemical fertilizer (N, P, K = 0·6, 0·39, 0·67 g pot⁻¹) was topdressed at 2-week intervals after transplanting. A water depth of 2–3 cm was maintained in flooded treatments. In aerobic30 and aerobic80 treatments (which differed in cyclical drying cycles), full irrigation was applied when the soil water potential at 15-cm depth reached –30 and –80 kPa, respectively. Free water was immediately drained from small holes at the bottoms of the pots. One day before measurement of water-uptake (see below), full irrigation was applied to aerobic treatments and the soil was kept saturated during the measurements.

Measurements

Ψ_soil was measured in the field experiment at one position in one replicate each of the aerobic and saturated treatments. Porous-cup tensiometers (DIK-8333; Daiki Rika Kogyo, Saitama, Japan) were installed at 20- and 40-cm soil depths (Watermark 200SS soil moisture sensors; Irrometer Company, Riverside, CA, USA) were installed at a depth of 5 cm. The groundwater levels in aerobic and saturated treatments were monitored using piezometers (open-bottom PVC tubes installed to a depth of 100 cm).

To monitor canopy growth non-destructively, the fraction of radiation intercepted weekly by each replicate was measured by using a linear photosynthetically active radiation receptometer (AccuPAR; Decagon Devices Inc., Pullman, WA, USA). Stomatal conductances (g_s) of leaf abaxial sides were measured in six to eight plants per plot by using an SC-1 leaf porometer (Decagon Devices, Inc.) in the morning (1000–1200 h) under clear conditions. Ψ_leaf was also measured at pre-dawn (0100–0400 h) and midday (1200–1500 h) in two or three plants per plot by using a pressure chamber (DIK-7002; Daiki Rika Kogyo) at 58, 69, 77 and 89 d after sowing in 2009. The topmost fully expanded leaf of the largest stem on a plant was selected for measurements of g_s and Ψ_leaf.

Dynamics of root morphology were monitored in 2009 by the core sampling method (Henry et al., 2011; Kato and Okami, 2010). Four soil cores were taken from each plot with a soil sampler (5-cm diameter, 35-cm long; DIK-110B, Daiki Rika Kogyo) at the mid-position between rows. Few rice roots grew below 35 cm. Samples were washed with a gentle stream of water on a 0·5-mm-mesh screen. After debris had been removed, an 8-bit greyscale image of each fresh root sample was acquired by digital scanning at a resolution of 400 dpi with a flatbed image scanner (Epson Expression 10000XL; Epson America, Inc., San Jose, CA, USA). The root lengths in TIFF images were analysed with commercial software (WinRHIZO v. 2009b; Regent Instruments, Montreal, QC, Canada). To avoid underestimation of fine root lengths during image processing, the threshold for separating roots from background was adjusted automatically in ‘Lagarde's mode’ in WinRHIZO (Kato et al., 2010). WinRHIZO was also used to estimate root diameter distributions. After samples had been oven-dried at 80 °C for 72 h, roots were weighed and specific root lengths (ratio of root length to root weight) were calculated. An elevated specific root length indicates an efficient fine-root proliferation for a given allocation of assimilates to roots. A diameter of 0·2 mm was designated as the threshold separating thick and fine roots. Using this definition, most adventitious roots are classified as thick roots, while almost all lateral roots are classified as fine roots (Kato et al., 2010; Henry et al., 2011). The fine : thick root length ratio, which is a representation of the lateral root length to adventitious root length ratio, was then determined.

Transpiration characteristics and plant growth were measured in the pot experiment 61 d after transplanting. One of the two pots in each plot was used for measurement of water uptake, and the other was used for measurement of Ψ_leaf. Water-uptake rate was determined by weighing pots at 2-h intervals from 0600 to 1800 h. It was assumed that plant transpiration reached hydraulic steady state from 1000 to 1200 h, when the water-uptake rate was at its daytime maximum (data not shown). To prevent evaporation, pot surfaces were covered with plastic wrap and aluminium foil. Ψ_leaf, g_s and SPAD (a measure of chlorophyll content) were measured on three or four of the largest stems per hill from 1000 to 1200 h; chlorophyll contents were determined with a SPAD-502 chlorophyll meter (Minolta Co., Ltd, Osaka, Japan). Leaf area was measured with an area meter (LI-3100; LI-COR, Lincoln, Nebraska, USA) and shoot dry weight was determined after drying in an oven at 80 °C for 3 d. Root length was also determined as described above after counting the number of adventitious roots.

From water-uptake data, whole-plant conductance of hydraulic water flow from root systems to leaves (whole-plant hydraulic conductivity, K_pa) was calculated according to an Ohm's law analogy of water flow (Tomar and O'Toole, 1982; Hirasawa and Ishihara, 1991; Stiller et al., 2003):

A mathematical equation, expression, or formula.
Object name is mcr184eqn1.jpg

(1)

where, E_leaf is the transpiration rate per unit leaf area from 1000 to 1200 h. Ψ_soil values of flooded and saturated soils were set to zero for calculation purpose.

Hydraulic conductance normalized by total root length (root hydraulic conductivity, L_p) was calculated as follows (Adachi et al., 2010, 2011):

A mathematical equation, expression, or formula.
Object name is mcr184eqn2.jpg

(2)

where, E_plant is the transpiration rate per hill from 1000 to 1200 h and L is total root length.

Data from all trials in each experiment were analysed by analysis of variance (SAS Institute, 2003). Fisher's LSD (least significant difference) test was used for post hoc comparisons of treatment means.

RESULTS

Soil moisture conditions and canopy growth in the field experiment

In the aerobic treatment, Ψ_soil at 20-cm depth usually stayed above –30 kPa (Fig. 1). In aerobic treatments, Ψ_soil stayed slightly lower at 5-cm depth and slightly higher at 40-cm depth than at 20-cm depth. In the saturated treatment, Ψ_soil at 20-cm depth was usually between –5 and –10 kPa, and above –20 kPa at 5-cm depth. Groundwater levels in aerobic and saturated treatments were below 90 cm, except briefly after heavy rainfall (data not shown). The time courses of fractions of radiation intercepted indicated differences in early vigour among treatments; canopies expanded more rapidly at the vegetative stage in flooded than in the aerobic soils (Fig. 2). There was no difference in early vigour between aerobic and saturated treatments.

Fig. 1.

Time courses of soil water potentials in saturated and aerobic treatments (field experiment; means ± s.e., n = 3; some error bars are hidden by symbols).

Fig. 2.

Time courses of fractions of radiation intercepted by canopies in the different water regimens in 2009 (means ± s.e., n = 3; most error bars are hidden by symbols). Bars below the plots indicate Fisher's LSD (P = 0·05).

Stomatal conductance and leaf water potential in the field experiment

g_s in the saturated treatment was not significantly different from that in the flooded treatment during crop growth (Fig. 3). g_s in the aerobic treatment was lower than or similar to that in the flooded treatment. g_s in the aerobic treatment decreased with decreasing soil moisture (Fig. 4). g_s in saturated and aerobic treatments relative to that in the flooded treatment was negatively associated with soil water tension (negative values of Ψ_soil) at 20-cm depth, although there were large g_s variations at each water tension value. g_s differences between aerobic and flooded conditions were not apparent when soil water tension at 20-cm depth was <15 kPa. The curvilinear fit (Fig. 4) shows that there was a 17 % reduction in g_s to that in the flooded treatment when soil water tension at 20-cm depth was 20 kPa in the aerobic treatment.

Fig. 3.

Time courses of stomatal conductance in different water regimens (means ± s.e., n = 3; most error bars are hidden by symbols). Bars below the plots indicate Fisher's LSD (P = 0·05).

Fig. 4.

Relationship between soil water tension at 20 cm and relative stomatal conductance (under saturated and aerobic/flooded conditions). Bars indicate standard errors (n = 3). **P < 0·01.

Midday Ψ_leaf was significantly lower in the saturated treatment than in the flooded treatment (Fig. 5). Ψ_leaf values were not significantly different between saturated and aerobic treatments when Ψ_soil at 20 cm was not less than –15 kPa. Although the difference was not significant, Ψ_leaf slightly decreased in the aerobic treatment compared with the saturated treatment when Ψ_soil was –20 kPa (58 d after sowing). Pre-dawn Ψ_leaf values in the aerobic treatment were –0·06 to –0·07 MPa and little different from values in flooded and saturated treatments (> –0·05 MPa). There was no relationship between relative g_s (ratio under saturated or aerobic conditions/flooded condition) and the difference in midday Ψ_leaf between flooded, saturated and aerobic treatments; a reduction in Ψ_leaf occurred in saturated and aerobic treatments even when g_s was unchanged (data not shown).

Fig. 5.

Midday leaf water potential (Ψ_leaf) under different experimental water regimens (field experiment; means ± s.e., n = 3). Different lower-case letters indicate significant differences between means (Fisher's LSD; P < 0·05). (more ...)

Root morphology dynamics in the field experiment

Total root length density in the saturated treatment was 16–28 % of that in the flooded treatment (Fig. 6A). Thick root length density was also highest in the flooded treatment, reaching 2–3 times the values in the saturated treatment (Fig. 6B). Moreover, the difference among treatments in specific root length and in the fine : thick root length ratio became more obvious as plants grew; values were 140–170 % higher in the flooded treatment than in the saturated treatment when plants reached the reproductive stage (Fig. 6C, D). There were no differences between saturated and aerobic treatments in any of the root morphological traits (including total root-length density).

Fig. 6.

Time courses of total root length density (A), specific root length (B), thick root length density (C) and fine : thick root ratio (D) in the different water regimens (means ± s.e., n = 3). Bars indicate LSD (P = 0·05).

Root hydraulic conductivity and root morphology in the pot experiment

Different intensities of cyclical soil drying were imposed in the aerobic30 and aerobic80 treatments (Fig. 7). No drought stress symptoms (leaf rolling or drying) were observed, even in the aerobic80 treatment. Treatment effects on the transpiration rate per unit leaf area were not discernable at 61 d after transplanting (data not shown). Similarly, g_s was not different between treatments either (Table 2). However, Ψ_leaf was significantly lower in aerobic treatments than in the flooded treatment. Likewise, K_pa was lower in aerobic treatments than in the flooded treatment, although the difference between flooded and aerobic80 treatments was not significant. In contrast, L_p was slightly higher in aerobic treatments than in the flooded treatment (not significant).

Fig. 7.

Time courses of soil water potential at 15 cm depth in aerobic30 and aerobic80 treatments (pot experiment; means ± s.e., n = 5). In aerobic30 and aerobic80 treatments, irrigation was applied when the soil water potential reached –30 kPa (more ...)

Table 2.

Leaf water potential, stomatal conductance and plant hydraulic conductivity in the different water regimens (pot experiment)

Total leaf area was significantly different between treatments (Table 3), but other leaf characteristics related to transpiration, including specific leaf area and SPAD value, were not (data not shown). The effect sizes of water regimens were similar for leaf area, stem number, shoot and root dry weight, i.e. reductions to 62–70 % in aerobic30, and 47–68 % in aerobic80 of values in the flooded treatment. Reduction in total root length in aerobic treatments was more marked (reduced to 32–43 % of values in the flooded treatment; Table 4). Root number was halved in aerobic treatments in comparison with the flooded treatment; however, individual adventitious root growth was greater in aerobic treatments than in the flooded treatment (128–141 % of flooded treatment values). Specific root length and fine : thick root length ratio were significantly lower in aerobic treatments than in the flooded treatment.

Table 3.

Leaf characteristics, shoot dry weight and root dry weight in the different water regimens (pot experiment)

Table 4.

Root growth characteristics in the different water regimens (pot experiment)

DISCUSSION

High yield and high crop water productivity are attainable in water-saving rice cultivation when high-yielding cultivars are used with appropriate management (Kato et al., 2009; Sudhir-Yadav et al., 2011). However, rice is susceptible to soil water deficit and yield is unstable in aerobic culture; e.g. grain yield in the aerobic treatment was very high (>9 t ha⁻¹) in both years, but still 20 % lower than in the flooded treatment in 2009 (Okami et al., 2009). It was demonstrated that a range of –15 kPa to –20 kPa at 20-cm depth is a threshold for maintaining transpiration in aerobic soils (Fig. 4). Note that the value is considerably high compared with other dryland crops (Lafitte and Bennett, 2002). Once Ψ_soil dropped below the threshold, it reduced Ψ_leaf and thereby g_s concomitantly. Accordingly, development of new rice cultivars resilient to moderate soil water deficit is required for the implementation of water-saving irrigation (Serraj et al., 2011). The relationship between Ψ_soil and Ψ_leaf is mediated by rooting depth in aerobic rice culture (Kato and Okami, 2010), suggesting that genetic improvement aimed at deeper rooting would be an effective goal. This suggestion has recently been supported by performance evaluations of advanced IR64 (an elite indica cultivar) backcrossed lines differing in rooting depth and tested under aerobic rice culture conditions with various irrigation intensities (Kato et al., 2011).

g_s and Ψ_leaf are co-regulated in plants as an adaptation to environmental fluctuations (Boyer, 1996; Tardieu and Simonneau, 1998; Damour et al., 2010). It was shown that Ψ_leaf is significantly reduced even under saturated conditions, whereas the relative g_s value was maintained whenever Ψ_soil was above –15 kPa (Figs 4 and and55 and Table 3). This is noteworthy because previous studies suggest that rice has a conservative response to drought stress, i.e. g_s controlled in such a way that Ψ_leaf is maintained under soil water deficit (Parent et al., 2010); the g_s control mechanism is triggered in part by non-hydraulic signals such as abscisic acid (Siopongco et al., 2009). These processes highlight the difference in rice response between well-watered aerobic conditions and drought conditions. Reduction in Ψ_leaf causes slower leaf expansion, limited radiation capture during the vegetative stage and reproductive failure, as depicted in Fig. 2 (Boyer, 1970; Ehlert et al., 2009). For aerobic cultivation of high-yielding rice, altering the plant leaf ‘opportunistic strategy’ of gas exchange to maximize photoassimilation through introduction of suitable genes conferring a sensitive stomatal behaviour to relieve the reduction in Ψ_leaf might be advantageous (O'Toole and Cruz, 1980; Tomar and O'Toole, 1982; Dingkhun et al., 1989).

The relationship between hydraulic water flow and the gradient between Ψ_soil and Ψ_leaf may be considered a function of whole-plant conductance (as shown in eqn 1) when hydraulic resistance in the soil is negligible (i.e. Ψ_soil > –40 kPa; Blizzard and Boyer, 1980; Gardner and Ehlig, 1962). Theoretically, a reduction in Ψ_leaf is caused either by reduction in transpiration rate or whole-plant hydraulic conductivity (K_pa), according to eqn (1) (Stiller et al., 2003). Ψ_leaf may reduce even if K_pa is not significantly changed, while the lower Ψ_leaf would occur when K_pa reduces under well-watered aerobic condition compared with flooded conditions (Fig. 5 and Table 2). K_pa is determined mostly by conductance of water transport below ground (Boyer, 1969; Hirasawa and Ishihara, 1991; Steudle and Peterson, 1998), although the occurrence of xylem embolism in transpiring plants (Domec et al., 2006; Stiller et al., 2003) cannot be ruled out. Accordingly, when K_pa becomes lower in the aerobic treatment compared with the flooded treatment, it would largely be the result of differences in the hydraulic conductance of the root systems. These observations are in accord with a previous study demonstrating that the hydraulic conductance of root systems of rice grown under well-watered aerobic conditions (Ψ_soil = –33 kPa) were much lower than that under flooded conditions, though this was not the case for leaf and stem hydraulic conductances (Tomar and Ghildyal, 1975).

As the axial hydraulic conductance of a root is much larger than the radial conductance (Steudle, 2000), hydraulic conductance of the whole root system can be divided into two components: total root length (or total root surface area) and root hydraulic conductivity (L_p) (Adachi et al., 2010, 2011; Hirasawa et al., 1992). L_p was slightly higher under well-watered aerobic condition than under flooded conditions in this study (Table 2), while it generally decreases under soil water deficit causing further reduction in K_pa under drought stress (Cruz et al., 1992; Matsuo et al., 2009). These considerations of the present work and that of others suggested that lower Ψ_leaf values in aerobic rice culture than in flooded rice culture are attributable, at least in part, to poorly developed root systems, even under well-watered aerobic conditions. In commercial paddy farming, rice genotypes with small rooting sizes would have significantly reduced K_pa values (Jiang et al., 1988; Adachi et al., 2010), an effect that would not be detectable in young seedlings. L_p was indirectly estimated in this study instead of pressurizing the whole root system in a pressure chamber (Wan et al., 1996; Miyamoto et al., 2001; Matsuo et al., 2009). While the suction induced by transpiration is hard to control, the estimation of L_p with the aid of an analogy of Ohm's law (eqn 1) was accurate enough to detect the genomic regions conferring higher hydraulic conductance and photosynthetic rate in rice (Adachi et al., 2011).

The restricted root system development in the saturated treatment (Fig. 6) indicates that rice root growth is mediated directly by aerobic conditions when plants are grown in water-saving culture, as well as by soil water deficit. Root system architecture in rice is a function of adventitious root growth (from the base of the stem) and of lateral root branching on each adventitious root (Rebouillat et al., 2009). As postulated previously (Kato and Okami, 2010; Kato et al., 2010), these two morphological components of root system architecture are the primary determinants of total root length down-regulation under aerobic conditions (Fig. 6 and Table 4). Although the length and weight of each adventitious root are enhanced under aerobic conditions, this does not fully compensate for reduced adventitious root emergence and lateral root branching. Interestingly, adventitious root emergence in rice plants is up-regulated under hypoxia stress facilitated by the death of epidermal cells at the stem nodes external to the root primordia (Mergemann and Sauter, 2000). These processes were promoted by ethylene and suppressed by abscisic acid (Steffens and Sauter, 2005). Furthermore, there is a substantial increase in root mechanical impedance in plants under soil water deficit due to changed root anatomy, i.e. thickened cell walls and accelerated lignification of endodermis, exodermis and sclerenchyma (Taleisnik et al., 1999; North and Nobel, 2000). These changes are viewed as adaptations to increased soil dryness and mechanical impedance (for a review, see Enstone et al., 2003). A similar alteration in root anatomy occurs in rice plants grown in well-watered aerobic fields (Mostajeran and Rahimi-Eichi, 2008; Y. Kato, pers. obs.), indicating that rice roots are more sensitive to water management than are the roots of dryland crops. Rice roots appear to respond to aerobic conditions as though they were under drought stress. Since lateral roots differentiated from the pericycle of adventitious roots must penetrate through outer cell layers, including endodermis, exodermis and sclerenchyma, changes in root anatomy may impede lateral root branching in water-saving culture (Péret et al., 2009), as is the case with the effect of sulphide toxicity on rice roots (Armstrong and Armstrong, 2005). The underlying mechanism of the lateral root branching response to anaerobic/aerobic conditions remains unknown and awaits further investigation.

Conclusions

The two morphological components of the rice root system, i.e. adventitious root emergence and lateral root proliferation were down-regulated under aerobic culture conditions, resulting in a significant decrease in total root length in this mode of cultivation. When soil-leaf hydraulic conductance became lower in rice plants grown in aerobic than in those grown in flooded culture due to considerably reduced rooting size, it had a negative impact on Ψ_leaf even under nearly saturated conditions. g_s was unchanged when the soil moisture was at around field capacity, while it was inevitably reduced when the soil water potential at 20-cm depth reached –20 kPa. The reduction in Ψ_leaf often leads to a significant yield loss through the detrimental effect on canopy expansion and/or reproductive growth. Therefore, we suggest that constitutively shallow rooting and sensitive responses of rhizogenesis and lateral root branching to unsaturated soils are the main reasons why rice has limited adaptability to water-saving aerobic culture. There are potential opportunities for genetic adaptation to aerobic conditions through isolation and insertion of genes responsible for enhanced adventitious root emergence and lateral root proliferation under aerobic conditions.

ACKNOWLEDGEMENTS

We thank K. Ichikawa, R. Soga, and K. Yatsuda (University of Tokyo) for their technical assistance in carrying out these experiments. This work was supported in part by a Grant-in-Aid for Scientific Research (No. 20780010) from the Japan Society for the Promotion of Science (to Y.K.).

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