J Intl Cooper Agric Dev 2020; 18: 48–55

Journal ofInternational Cooperation for
Agricultural Development

Working Paper

Enhanced Root System Development
Responses of a Newly Identified Mutation
Gene Promoting Lateral Root Development
to Various Nitrogen Conditions in Rice
Nonawin Lucob-Agustin1), Tomomi Hasegawa1), Kyosuke Jinno1), Roel R. Suralta2),
Jonathan M. Niones2), Mana Kano-Nakata3), Akira Yamauchi2) and Yoshiaki Inukai3)
1) Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Aichi 464-8601, Japan

2) Philippine Rice Research Institute, Central Experiment Station, Science City of Muñoz, Nueva Ecija, 3119, Philippines
3) International Center for Research and Education in Agriculture, Nagoya University, Nagoya, Aichi 464-8601, Japan

Received December 10, 2019 Accepted January 17, 2020
Abstract. Lateral roots (LRs), which largely constitute the root system, allow the entire root system to expand to a larger
area to efficiently capture water and nutrients from the soil. Thus, the optimization of LRs should be considered for the
genetic improvement of root system architecture to most notably impact plant acquisition of soil resources for productivity.
In this study, we newly identified a rice mutant, 11NB10, which has a high number of thick, long, and highly branched LRs(L-type LRs) with promoted parental root growth. We evaluated the root performance of this mutant under various nitrogen(N) regimes, including 30, 60, and 120 mg N corresponding to low, standard, and high N conditions, respectively. The
results showed that under low N conditions, the 11NB10 mutant had a larger root system based on its total root length, which
increased further with increasing N levels, compared to its wild-type, Nipponbare. This promoted root system growth could
be attributed to the development of highly branched L-type LRs, which in turn might contributed to higher leaf area and shootdry matter production. These findings suggest that the 11NB10 mutation gene promotes a highly developed root system under
low N conditions, and its root performance could be further improved by enhancing LR development through N application.
Thus, the 11NB10 mutant is a promising line for the breeding programs targeting root system architecture in rice.
Key words: rice, lateral root, nitrogen, root system architecture, mutant

Introduction
Rice (Oryza sativa L.) is consumed as a staple cereal
crop by half of the world’s population1) and is cultivated onover 150 million ha of land globally. However, the recent
climatic conditions pose serious risks to rice production,
thereby threatening food security2). Irrigated rice fields,
where water-saving technology (alternating wet and dry
conditions) is practiced, and less favorable environments,
Corresponding author: Y Inukai, e-mail: inukaiy@agr.nagoya-u.
ac.jp

48 J Intl Cooper Agric Dev 2020

such as rainfed lowland or upland ecologies, are more vulnerable to variable weather events, leading to constrained
rice production in these areas3, 4). In such uncertain situations, optimizing root system architecture has been suggested as a rational strategy to improve nutrient and wateracquisition5) in plants and, thus, to achieve food security.
The root system architecture in rice is determined by
the overall growth and angle of its various components,
including the seminal, crown, and lateral roots (LRs)6, 7).
Being the root component that constitutes approximately
90% of the root system, the LRs predominantly determine
the overall function of the root system8) in a large variety

of environmental and soil nutrient conditions to optimize
plant growth, adaptation, and productivity9, 10). In rainfed
lowland fields in developing countries, wherein a hardpan
is located approximately 20 cm below the soil surface11, 12),the roots are almost entirely restricted to water and nutrients found above the hardpan. It was reported that insuch cases, the branching and elongation of LRs contributed greatly to the total root length, which consequently
produced greater total dry matter, especially under mild
drought stress13). Further evidence was provided that LR
production contributed to plant yield under soil moisturefluctuation regimes14). Additionally, the development ofa deeper root system and LR growth promotion at 30–45
cm soil depths as a response to periods of progressive
drought stress alleviated the effects of water deficit on
grain yield15), and similar root phenotype at the same soil
depth was likewise reported to maintain shoot dry matterproduction under progressive drought stress16). These root
characteristics are associated with increased root water
uptake and, to some extent, nutrient uptake. Furthermore,total root length development, which is contributed by LR
branching and elongation, could be enhanced by standard
and high nitrogen (N) applications. This, in turn, could leadto increased shoot growth under drought conditions17–19).
These results indicated that LR growth could be inducedby controlling the level of N in soils. In this regard, we
identified a rice mutant, 11NB10, that exhibits a highnumber of thick, long, and highly branched LRs (L-typeLRs) with normal and promoted parental root growth at
the seedling and higher growth stages.
In Philippines, the rainfed systems (upland and lowland)
cultivated for rice occupy 1.51 M ha of the 4.8 M ha totalrice production areas20). In 2018, these production areas
produced 3.12 mt yield ha-1, which is significantly lower
than their irrigated counterpart that produced 4.37 mt yield
ha-1. It is anticipated, therefore, that any improvement inthese production areas might contribute to the overall yield
increase performance of the country. As 11NB10 mutant
line showed promoted root system traits, we further used
this material to evaluate the utilization of its root traits
under various N regimes and their overall effect on shootdevelopment under Philippine conditions.

Pot experiment
The 11NB10 mutant and Nipponbare were evaluated ina pot experiment conducted in a glasshouse located on thecampus of Nagoya University, Nagoya, Japan (35°6′42′′
N, 137° 4′57′′ E) from July to August 2017. The seeds ofthe 11NB10 mutant and Nipponbare were pre-germinatedusing tap water mixed with fungicide (benomyl benlate,
0.15% w/v) and incubated in a growth chamber maintained
at 28°C under continuous light. The pre-germination of the
11NB10 mutant occurred 2 days earlier than the wild-type
plants sowed at the same time (wild-type: 3 days; mutant:
5 days). Three pre-germinated seeds from each line weresown in a 1/5,000 Wagner pot (16 cm diameter, 20 cm
height) filled with 4.0 kg air-dried sandy loam soil. The
soil in each pot was pre-mixed with fertilizer at the rate of
60-60-60 kg ha–1 NPK. The seedlings were later thinned to
one seedling per pot at 10 days after sowing (DAS) withwater level maintained at 2 cm above the soil surface until
the termination of the experiment.
Rootbox experiment
Time and Location

This experiment was conducted in a screenhouse at the
PhilRice Central Experiment Station (PhilRice-CES), Science City of Muñoz, Nueva Ecija, Philippines (15°40′ N,
120° 53′E, 57.6 m altitude) between January 15, 2019 toFebruary 22, 2019.
N Treatments and Plant SamplingMaterials and Methods

Two plants each of the 11NB10 mutant and Nipponbare
were targeted to be grown at both sides of a polyvinyl
chloride (PVC) rootbox (25 cm × 2 cm × 40 cm, L × W
× H)21). Firstly, six pre-germinated seeds, i.e., three seeds
each of the 11NB10 mutant and Nipponbare, were sownat approximately 5 cm away from both ends of the PVC
rootbox (Fig. 3a). The seedlings were later thinned into
one seedling each of the PVC rootbox sides after 5 DAS.
As described previously13, 18, 22), three different levels of
N fertilizer (urea: 46% N), including 30 (low), 60 (standard), and 120 mg (high), each thoroughly mixed with 80
mg phosphorus (single superphosphate: 17.5% P2O5) and
70 mg potassium (KCl: 60% K2O), were added into 2.5 kg
air-dried soil per rootbox prior to seed sowing.

Plant Materials

Physiological Measurements

The rice mutant, 11NB10, and its wild-type, Nipponbare, which differ in root system development, were
utilized in the study. The 11NB10 mutant is an N-methylN-nitrosourea (MNU)-induced mutant, in which the rootsystem development is more promoted compared to Nipponbare.

Leaf photosynthesis of the second youngest fully-expanded leaf was measured using a portable photosynthesis
system (Li-6800, LiCOR Inc., Lincoln, Nebraska, USA)starting at 1000 h. The relative chlorophyll content wasmeasured using a chlorophyll meter (Soil and Plant Analysis Development, SPAD-502, Minolta) and expressed as
J Intl Cooper Agric Dev 2020 49

SPAD value. All measurements were performed at 36
DAS, two days before the termination of the experiment.
Shoot and Root Growth Measurements

Sampling was performed at 38 DAS. The shoots were
cut at the stem base and oven-dried at 70°C for 2 days
prior to the recording of the dry weight. The roots were
sampled using a pinboard and transparent perforated
plastic sheet as described previously21, 23). The extracted
root systems embedded in plastic sheets were stained with
0.25% Coomassie Brilliant Blue R 250 aqueous solution
for at least 24 h. This staining procedure was indispensablefor taking high-resolution digital scans of the entire rootsystem, including the fine LRs, using an A3-size scanner(EPSON 10000G) at 300 dpi. Subsequently, the total
number of crown roots was manually counted, and theroot samples were stored in 95% ethyl alcohol for further
measurements. For root length measurements, the roots
were cut, spread on transparent glass trays with minimal
overlapping and scanned at 600 dpi with a pixel thresholdvalue of 175 using an A4-size scanner (EPSON 4990).
The scanned images were analyzed for root length using
the WinRhizo software (Régent Instruments, Québec,Canada) and categorized according to LR diameter. Previ-

ously, LRs have been classified into two types according
to diameter and length, the S-type and L-type LRs. The
L-type LRs are thick, long, and branched into the higherorder LRs, whereas the S-type LRs are slender, short, andnon-branching24). The LRs with diameter sizes of 0 < 0.08
and 0.08 ≤ 0.30 mm were classified as thin and thick,respectively25).

Results
11NB10 mutant selection and performance undersoil conditions

The 11NB10 mutant was observed to have a promoted
root system compared to its wild-type, Nipponbare, under
tap water conditions at the seedling stage (Fig. 1a-b). The
mutant had remarkably longer parental roots and higher
number of long and thick LRs (L-type LRs), but the sameLR density and number of crown roots as that of the wild
type (Fig. 1c-f); thus, it was selected as plant material in
our study. These root development differences were consistently observed under soil conditions using pot set-up
at the maximum tillering stage (Fig. 2a-b). The whole rootsystem of the 11NB10 mutant appeared to have longer parental roots and highly branched LRs despite the observed

Fig. 1. Root morphological features of 11NB10 mutant at seedling stage.

Shoot and root system of Nipponbare (a) and 11NB10 mutant (b) and their roots traits (c–f) at 15 days after germination
grown under tap water conditions. Values represent means ± SE (n=10). ** and *** indicate statistically significant at P<0.01
and P<0.001 in the means between genotypes as revealed by two-tailed Student’s T-test, respectively (ns, non-significant).

50 J Intl Cooper Agric Dev 2020

Fig. 2. Shoot and root system profiles of 11NB10 mutant plants under soil conditions at maximum tillering stage.

Pot experiment set-up in a glasshouse (a) to evaluate shoot phenotypes (b), shoot traits (c–f), entire root system formation(g) and root traits (h–j) of Nipponbare (left) and 11NB10 mutant (right) grown in soil supplied with 60-60-60 kg ha–1 NPK
under irrigated conditions at maximum tillering (65 days after sowing). Values presented for total shoot dry weight, total root
length, total CR and LR length were ratio of the whole plant traits to the stem number for direct comparison of these traits.
CR, crown root; LR, lateral root. Values represent means ± SE (n=4). * and ** indicate statistically significant at P<0.05
and P<0.01 in the means between genotypes as revealed by two-tailed Student’s T-test, respectively (ns, non-significant).

lower number of parental roots from the base (Fig. 2g),
which was due to the reduced stem number as shown in
Fig. 2b. Because of these differences in stem number (Fig.
2c), the shoot and root traits were directly compared byobtaining the ratio of the trait to the stem number, and we
found that the shoot dry weight of the 11NB10 mutant
was not negatively affected by the mutation (Fig. 2e). In
addition, the 11NB10 mutant had taller plant height andcomparable net photosynthesis to the wild-type Nipponbare (Fig. 2d, f), revealing that the mutation negatively
affected the stem number only of the shoot part. Notably,
the total root length and total LR length per stem numberof the 11NB10 mutant were significantly higher than
the wild type (Fig. 2h, j), while their crown root lengths
were similar (Fig. 2i), confirming that the gene mutation
promoted root system development through enhanced LR
development despite negatively affecting the stem numberof the shoot part.
Shoot and root system developmental responses of
the 11NB10 mutant under various N conditions

The 11NB10 mutant performance was further evalu-

ated under various N conditions (low, standard, and highN) following the same treatment method as described
previously13, 18, 22). N is the mineral nutrient required in
the greatest amount, and its availability is a major factor
limiting growth, development, and yield26). To precisely
evaluate the root system development differences of the
11NB10 mutant and Nipponbare, the rootbox-pinboard
method was utilized to collect the whole root system withminimal damage and preserve the resulting root architecture (Fig. 4)21–23). Furthermore, because of the differencesin the stem number between the 11NB10 mutant and wildtype, the tiller outgrowth was cut to maintain the growthof the main stem (Fig. 3b) during the entire duration ofplant growth, making the direct comparison of the shootand root traits feasible.
The net photosynthesis and SPAD value of the 11NB10
mutant and Nipponbare did not differ (Fig. 3c-d), whereas
the plant height and leaf area were significantly higher inthe 11NB10 mutant than in Nipponbare (Fig. 3e-f) under
different N conditions. On the other hand, the shoot dry
weight of the 11NB10 mutant was slightly higher than
Nipponbare at low and standard N levels and was signifiJ Intl Cooper Agric Dev 2020 51

Fig. 3. Shoot phenotypes of Nipponbare and 11NB10 mutant plants with main stem only under different nitrogen (N) conditions.

Plants grown in a root box at a screenhouse (a), the cutting of tiller outgrowth to maintain the main stem only for directcomparison of traits between Nipponbare and 11NB10 mutant (b) and their physiological (c–d) and shoot traits (e–g) at 38
days after sowing. Values represent means ± SE (n=5). *, ** and *** indicate statistically significant at P<0.05, P<0.01 andP<0.001 in the means between genotypes within each N treatment as revealed by two-tailed Student’s T-test, respectively(ns, non-significant).

Fig. 4. Root system profiles of Nipponbare and 11NB10 mutant plants at different nitrogen (N) conditions.

Root system profiles of Nipponbare and 11NB10 mutant grown under different N conditions (low,standard, high N) for 38 days. The intact whole root system was extracted from a rootbox using apinboard20, 16). Prior to taking digitized photographs in a scanner, the root system were stained with
0.25% Coomassie Brilliant Blue R solutions for at least 24 h.

52 J Intl Cooper Agric Dev 2020

Fig. 5. Root system development of Nipponbare and 11NB10 mutant plants grown under different Nitrogen conditions.

Root lengths (a–c), number of crown roots (d), lateral root length according to diameter sizes (e–g) and root dry weight (h)of Nipponbare and 11NB10 mutant grown under different N conditions (low, standard, high N) for 38 days. Values representmeans ± SE (n=5). *, ** and *** indicate statistically significant at P<0.05, P<0.01 and P<0.001 in the means between
genotypes within each N treatment as revealed by two-tailed Student’s T-test, respectively (ns, non-significant).

cantly higher under high N level.
The root system profiles of Nipponbare and 11NB10
mutant grown under different N conditions are shown in
Figures 4 and 5. Under low and standard N conditions, thetotal root length of the 11NB10 mutant was significantly
greater than that of Nipponbare, and it increased underhigh N level (Fig. 4 and 5a). The total root length of the
11NB10 mutant was significantly higher than that of Nipponbare by 8.3% and 22.5% at low and high N conditions,
respectively. Between the crown root lengths and LR
lengths that comprised the total root length, the lengthsof the LRs were more promoted than those of the crownroots and further enhanced under higher N conditions(Fig. 4 and 5b-c). The LR length of 11NB10 mutant wassignificantly higher than that of Nipponbare by 10.6% and25.7% at low and high N conditions, respectively, suggesting that the enhanced root system development of the
11NB10 mutant was due to greater LR development andits response to N level. Furthermore, the LR lengths werecategorized into different diameter sizes: thin, middle, andthick corresponding to the diameters sizes of 0 <D ≤0.08
mm, 0.08 mm <D ≤0.15 mm, and 0.15 mm <D ≤0.30
mm, respectively. The 11NB10 mutant showed greater
LR lengths because of the LRs with thick diameter sizes,
which are capable of higher order of branching (Fig. 5e-g)and, thus, a highly branched root system. In addition, themutant had significantly higher root dry weight than Nip-ponbare at all levels of N (Fig. 5h), while its crown root
number was higher only at high N level (Fig. 5d).

Discussions
The ability of rice plants to promote root system development, especially LR development, is a favorable trait
to efficiently acquire water and nutrients from a larger
soil area for productivity, given the highly dynamic soil
environments due to the changing climatic conditions persisting in agricultural areas9). This root characteristic wasassociated with the 11NB10 mutant that showed highly
branched root system under various N conditions (fromlow to increasing N levels), resulting in higher shoot dry
matter production than Nipponbare. Remarkably, the rootsystem of the 11NB10 mutant was further enhanced underhigh N level based on its total root length, which was
greatly contributed by LRs with the thick diameter andbranching (L-type LRs). Promoted LRs are linked to theenhanced uptake of N as well as other nutrients in different
crop species27–29), implying that these acquired nutrients
will be available for growth and development of the shootpart. Increasing N levels did not improve leaf chlorophyll
content and photosynthesis in the 11NB10 mutant, butcaused a slight increase in shoot dry weight, which could
be attributed to the higher number of main-stem leaves(data not shown) that contributed to greater leaf area. It
J Intl Cooper Agric Dev 2020 53

was reported that N is always distributed mostly to the
new growing organs, regardless of the growth stages of therice plant30). Thus, the absorbed N might be preferentiallyused in the expansion of developing leaves rather thanin increasing the chlorophyll content. Moreover, N canstimulate leaf synthesis and growth through the synthesisof proteins involved in cell growth, cell division, andcell wall and cytoskeleton synthesis31), thus leading to anincrease in the leaf area and hence in shoot dry weight.
The findings presented in this report might have implications for genetic improvement and breeding programsin rice that can be utilized under different rainfed lowland
and upland fields. The availability of this mutation genepromoting LR development is important for the improvement of root system architecture, and such mutation genecan be used more effectively by understanding proper N
levels to further improve LR growth. The root performance of this mutation gene further provides information
on natural resource and crop management practices32). Unlike in irrigated rice production system, wherein water isavailable in the fields, the rainfed lowland rice production
system is highly drought-prone and dependent on rainfall.
Thus, timely N application (i.e. after sufficient rainfall)should be considered to further improve the developmentof L-type LRs for a more vigorous root system, which willthen be useful for overcoming stressful conditions, suchas drought and soil moisture fluctuations, as demonstrated
in several studies9). Further work is required for evaluating the root performance of the 11NB10 mutant under
different water regimes (different drought intensities, soil
moisture fluctuations, upland conditions) and to further
elucidate the importance of promoted root response under
N fertilizer and then to water stress conditions.
Acknowledgements
We would like to thank Ms. Maria Corazon Cabral and
Ms. Antoinette Cruz for technical and administrative support, the staff of the Root Research team of PhilRice, Mr.
Rizal Romero, Mr. Victorino Salamanca, Mr. Albert Neri,
Mr. Albert Garcia, Mr. Oscar Ragasa, Mr. Daryl Gregorio,
Mr. Juanito Cortez and Mr. Hircoles Corpuz for their help
in the experimental operations and root processing. This
work was supported mainly by JSPS KAKENHI Grant
Number 18H02174.
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