increased grain yield and biomass allocation in rice under cool night temperature

ORIGINAL ARTICLE

Increased grain yield and biomass allocation in rice under coolnight temperature

Keiichi KANNO and Amane MAKINOGraduate School of Agricultural Science, Tohoku University, Sendai 981-8555, Japan

Abstract

The effects of different night temperatures on grain yield were examined in rice (Oryza sativa L. Akita-63) dur-

ing the ripening period. Plants were grown under two different night temperatures (22 and 27�C) from anthesis

to harvesting. The day temperature was maintained at 27�C in both treatments. Although the final biomass at

harvest did not differ between the treatments, the dry weight of the panicles was significantly greater in the cool

night temperature treatment. This increase in panicle weight was associated with increases in the 1000-kernel

weight and the ratio of filled spikelets. Although panicle respiration in the high night temperature treatment

decreased to almost zero just after the cessation of grain filling, the net CO2 fixation rate per day in the whole

plant in this treatment tended to be higher, and this was associated with a higher level of starch accumulation.

After grain filling, the starch content decreased and the final dry weight of other plant parts, including dead

organs and new tillers, was greater in the high night temperature treatment. Thus, the noted decline in yield at

the high night temperature led to changes in carbon allocation to new sinks for vegetative reproduction at the

whole plant level. From these results, we considered the possibility that a cool night temperature tends to favor

carbon allocation to panicles, resulting in higher yield.

Key words: biomass, grain yield, night temperature, Oryza sativa L, respiration.

INTRODUCTION

Rice (Oryza sativa L.) provides more food for humans

than any other crop. More than 90% of the world’s pro-

duction of rice is in Asia. Demand for rice is growing fas-

ter than the demand for other crops because population

increases are greatest in the rice-consuming regions of

Asia and Africa. However, several researchers have

pointed out that an increase in night temperatures from

global warming may reduce rice yields throughout the

world. Seshu and Cady (1984) predicted that rice yields

will decrease by 0.41 ton ha)1 (41 g m)2) when the aver-

age minimum daily temperature rises from 22 to 23�C.

Peng et al. (2004) reported direct evidence of decreases in

rice yields resulting from increased night temperatures

associated with global warming, with night temperature

strongly negatively correlated with grain yield. Ziska and

Manalo (1996) also observed a decline in the grain yield

of rice grown at a high night temperature. Similar results

were found by other researchers, that is, a negative corre-

lation between night temperature and grain yield in rice

(Morita et al. 2002, 2004, 2005; Sato and Takahashi

1971).

As rice is a tropical crop, yield is always higher in north-

ern Japan than in southern Japan (Murata 1964).

Although the reason for this difference is unknown, it is

possible that a difference in night temperature leads to the

difference in yield (Suzuki and Moroyu 1962). One possi-

ble explanation that has been considered is a carbohydrate

deficit caused by increased respiratory loss at high temper-

ature during the ripening period (Arashi and Tateishi

1950; Suzuki and Moroyu 1962; Sato and Takahashi

1971). However, Morita and co-workers recently

reported that the main factor for the decline in yield under

high night temperature was not an increase in respiratory

loss because no correlation between final grain weight and

whole plant biomass was found under different day ⁄ night

temperatures (Morita et al. 2002, 2004). Although their

experimental conditions for the day ⁄ night temperatures

(i.e. a regime of 22 ⁄ 34�C) were unnatural, the results of

Morita et al. (2004) suggest that an unknown factor

besides respiratory loss is related to the relatively low yield

in southern Japan. However, it is not still clear why grain

weight is not correlated with the whole plant biomass at

Correspondence: A. MAKINO, Graduate School of AgriculturalScience, Tohoku University, 1-1 Tsutsumidori-Amamiyamachi,Sendai 981-8555, Japan. Email: [email protected]

Received 28 July 2009.Accepted for publication 2 March 2010.

� 2010 Japanese Society of Soil Science and Plant Nutrition

Soil Science and Plant Nutrition (2010) 56, 412–417 doi: 10.1111/j.1747-0765.2010.00473.x

high night temperatures. Interestingly, Sato and Takah-

ashi (1971) observed a positive correlation between the

1000-kernel weight and the harvest index of rice growing

at different day ⁄ night temperatures. In addition, they

pointed out the possibility that a cool night temperature

increased the 1000-kernel weight. From their results,

however, it is difficult to evaluate the effects of night tem-

perature on grain yield because the grain yield depended

on both day and night temperatures.

The purpose of the present study was to elucidate the

effect of different night temperatures on grain yield and

biomass production of rice during the ripening period. We

grew rice plants hydroponically and transferred them to

temperature-controlled glasshouses under two different

night temperatures: 22 and 27�C. The day temperature

for all plants was maintained at 27�C. As previously

described (Kanno et al. 2009), the temperature of the

nutrient solution was also controlled using electric heaters

at the bottom of the plant pots. First we investigated the

allocation of biomass at the whole plant level at the

harvesting stage and examined the yield components of

the grains. Second we measured the rates of gas exchange

at the panicle and whole-plant levels. In addition, changes

in the amounts of carbohydrates were examined in the

stems during the ripening period. Finally, we discuss the

biological significance of a decline in rice yield under

elevated night temperatures.

MATERIALS AND METHODS

Plant culture and sampling

Rice (Oryza sativa L. cv Akita-63) plants were grown

hydroponically in a greenhouse following the procedure

used by Mae and Ohira (1981). Eight seedlings each were

transplanted to a 3.5-L plastic pot containing nutrient

solution. When the plants were heading, all plants were

moved into temperature-controlled greenhouses under

natural sunlight conditions (S-203A; Koito, Yokohama,

Japan) with two different night temperatures. One treat-

ment was set at 27�C during the day (05.00–19.00 hours)

and 22�C at night (cool night temperature [CNT]). The

other treatment was set at a constant 27�C (high night

temperature [HNT]). As reported previously (Kanno et al.

2009), because the water temperature of the nutrient

solution in the control in the morning is lower than the air

temperature, the solution was heated for 1 h from 04.00

to 05.00 hours with a 50-W heater attached to an

air-stone in the bottom of the pot. Thus, all plants were

grown under the same conditions during the daytime.

Four plants from each treatment were sampled between

11.00 and 14.00 hours 15, 30 and 45 days after anthesis.

Panicles, leaf blades, leaf sheaths, stems, roots and other

parts (containing dead parts and new tillers) were oven-

dried separately at 80�C for at least 3 days. The stems

were used to determine the sucrose and starch contents as

described previously (Nakano et al. 1995).

Yield components

Forty-five days after anthesis, the panicles from three pots

were collected and dried at room temperature for

3 weeks. Total panicle numbers per pot were in the range

of 21–26 (see Table 1). The panicles were hand-threshed

to determine the proportion of filled spikelets. The filled

spikelets were separated as they sunk in a NaCl solution

with a specific gravity of d = 1.06 (g cm)3). The sub-

merged spikelets were washed with water, hulled and then

oven-dried at 80�C to a constant weight to determine the

grain dry weight. The weight of the hulled grain was then

calculated as a moisture content of 15% to fresh weight.

Gas exchange rate of the whole plant

The gas exchange rate was determined using an environ-

mentally controlled growth chamber (Eyelatron FLI-

301NHL; Eyela, Tokyo, Japan) for the whole plant 15,

30 and 45 days after anthesis as described previously

(Kanno et al. 2009). The difference in the partial pressures

of CO2 entering and exiting the growth chamber was

measured continuously with an IRGA (LI-6252; Li-Cor,

Lincoln, NE, USA) and the absolute pressure of the CO2

was measured with another IRGA (ZRH; Fuji Electric,

Tokyo, Japan). Air was passed through soda lime to

remove the CO2 and mixed with a CO2 cylinder. The par-

tial pressure of CO2 in the chamber was adjusted to 37 Pa

and the flow rate through the chamber was maintained at

70 L min)1 (1.17 L s)1). Irradiance during the day was

800 lmol quanta m)2 s)1 at the center of the plant and

the temperature was set at the same temperature used

in the treatments. The respiratory rate of the panicles

was estimated by subtracting the dark respiration of the

Table 1 Yield components of rice grown at a night temperature of 22 or 27�C at the ripening stage (45 days after anthesis)

Temperature (�C)

Grain yield

(g pot)1)

1000-kernel

weight (g)

Filled

spikelets (%)

No. panicles

(no. pot)1)

No. spikelets

per panicle

CNT (27 ⁄ 22) 30.3 ± 0.7* 28.3 ± 0.1** 90.1 ± 1.6* 21.3 ± 0.3 55.8 ± 1.0

HNT (27 ⁄ 27) 25.4 ± 0.9* 26.0 ± 0.2** 80.9 ± 2.6* 23.7 ± 1.2 52.0 ± 1.0

Values are mean ± standard error (n = 3). *P < 0.05; **P < 0.01; CNT, cool night temperature; HNT, high night temperature.


Rice yield under cool night temperature 413

panicle-removal plants from that of the whole plants.

Dark respiration of the whole plant was first measured for

3 h, and then all panicles were removed and dark respira-

tion was measured again on the remaining tissue for 3 h;

the difference was regarded as an estimate of panicle

respiration.

RESULTS

Although the final biomass at the harvesting stage did not

differ between the treatments, the dry weight of the pani-

cles was appreciably greater in the CNT plants than in the

HNT plants (Fig. 1). However, the dry weight of other

parts was greater in the HNT plants. These parts included

dead organs and new tillers. The dry weight of roots also

tended to be greater in the HNT plants. Thus, a mild

increase in night temperature stimulated the growth of

new sinks, and led to a relative decline in biomass alloca-

tion in panicles. Figure 2 shows changes in the dry weight

of the panicles, stems and leaf sheaths during the grain-

ripening period. The dry weight of the panicle increased

more rapidly in the HNT plants in the first 15 days after

anthesis, and thereafter remained almost constant. In con-

trast, the dry weight of the panicles in the CNT plants

increased constantly over the ripening period. No clear

differences were found for changes in the dry weight of

stems and leaf sheaths between treatments. Thus, high

night temperature stimulated the rate of grain develop-

ment during the early stage of the ripening period, but

shortened the duration of the grain filling.

Grain yields were approximately 19% higher in the

CNT plants than in the HNT plants (Table 1). This

increase in yield in the CNT plants was associated with

increases in the 1000-kernel weight and in the ratio of

filled spikelets. No differences in panicle numbers and

spikelet numbers were observed between treatments.

Changes in the rates of CO2 uptake and dark respira-

tion were examined in the whole plant 15, 30 and 45 days

after anthesis (Table 2). Although the rate of CO2 uptake

did not differ between the treatments on day 15, it was

lower in the CNT plants than in the HNT plants on day

30. The rate of dark respiration rate was lower in the

CNT plants on day 15 and day 30, but net CO2 uptake

per day was still lower in the CNT plants on day 30. A

greater CO2 uptake in the HNT plants on day 30 may

have been a result of the development of new young

tillers. Figure 3 shows the changes in starch and sucrose

contents in the stems during the ripening period. Contrary

to CO2 uptake, starch accumulation was lower in the

HNT plants on day 30. As the dry weight of the panicle

did not increase in the HNT plants from day 15 after

anthesis (Fig. 2), a large decline in the starch content

between days 15 and 30 may have been the result of

the growth of young tillers. Changes in the sucrose con-

tent did not differ between treatments during the ripening

period.

Figure 1 Total dry weight and biomass allocation of rice grownunder night temperatures of 22 or 27�C at the ripening stage(45 days after anthesis). The biomass allocation to each organ isgiven as a percentage of the total shoot biomass. Values in paren-theses are standard errors (n = 3–4). Other contains dead organsand new tillers. The total dry weights of the cool night tempera-ture and high night temperature plants (including roots) were8.8 ± 0.2 and 9.0 ± 0.2 g plant)1, respectively.

Figure 2 Changes in the dry weight of panicles, stem and sheathof rice during the grain-filling period at night temperatures of 22or 27�C. Error bars indicate the standard error (n = 3–4). DAF,days after flowering.


414 K. Kanno and A. Makino

Finally, panicle respiration was determined. As it was

difficult to directly measure the respiratory rate of the

panicles, the rate was estimated by subtracting the dark

respiration of panicle-removal plants from that of the

whole plants. Panicle respiration did not differ between

the treatments on day 15, but decreased to almost zero

in the HNT plants on day 30 (Table 3). This means

that panicle respiration had no effect on the dry weight of

panicles in the HNT plants.

DISCUSSION

In agreement with previous studies, our results indicated

that a mild increase in night temperature during the ripen-

ing period led to a significant decline in grain yield (Fig. 1;

Table 1). This decline in yield was caused by declines in

both grain weight and the ratio of filled spikelets

(Table 1). Similar results were observed by Morita et al.

(2004). Conversely, Peng et al. (2004) attributed the

decline in yield at high night temperature to a reduction in

the total number of spikelets per plant. In the case of

Morita’s experiments and ours, because the temperature

treatments were imposed after anthesis, no differences in

spikelet number per panicle and panicle number per plant

were observed. Thus, when the plants were grown under

different night temperatures from the vegetative stages

through to anthesis, a decline in yield at high night tem-

perature might be caused by lower grain maturity as well

as a decrease in the spikelet number.

Morita et al. (2005) reported that high night tempera-

ture shortens the duration of grain development and

consequently results in a decline in final grain weight.

They also found a reduction in cell size between the

central point and the surface of the endosperm of the

grain, and considered the possibility of lower assimilate

supply to the grains at high night temperature. A shorten-

ing of the duration of grain development at high night

temperature may be related to an accelerated rate of

increase in grain weight. Kobata and Uemuki (2004)

reported that an early cessation of grain development is

likely to be caused by a shortage of the assimilate supply

to meet the requirements for increases in the grain growth

rate. In fact, early cessation of grain development was also

observed when a high night temperature was applied to

only the panicles (Morita et al. 2004; Nagato and Ebata

1960). However, Morita et al. (2004) found that the

decline in grain weight was greater when the whole plant

was exposed to a high night temperature rather than the

panicles alone. This suggests that the noted decline in

Figure 3 Changes in the starch and sucrose contents in thestems of rice during the grain-filling period at night temperaturesof 22 or 27�C. Error bars indicate the standard error(n = 3). *P < 0.05; **P < 0.01. DW, dry weight. DAF, daysafter flowering.

Table 2 Dark respiration and gross and net CO2 uptake inwhole plants grown at a night temperature of 22 or 27�C fromanthesis, 15, 30 and 45 days after anthesis

Temperature

(�C)

Dark

respiration

(nmol CO2

plant)1 s)1)

Gross CO2

uptake

(nmol CO2

plant)1 s)1)†

Net CO2

uptake

(nmol CO2

plant)1 s)1)‡

On anthesis

– 34 102 68

Day 15

CNT (27 ⁄ 22) 14 89 75

HNT (27 ⁄ 27) 21 91 70

Day 30

CNT (27 ⁄ 22) 4.6 21 16

HNT (27 ⁄ 27) 7.7 41 34

Day 45

CNT (27 ⁄ 22) 8.6 3.5 )5.1

HNT (27 ⁄ 27) 4.1 5.0 0.9

†Gross CO2 uptake is defined as the CO2 uptake actually measured dur-ing the day. ‡Net CO2 uptake is defined as the gross CO2 uptake minusdark respiration. Values are means (n = 2). CNT, cool night temperature;HNT, high night temperature.

Table 3 Dark respiration of the panicles and whole plantsgrown at night temperatures of 22 or 27�C 15 and 30 days afteranthesis

Temperature

(�C)

Panicle

(nmol CO2

plant)1 s)1)

Whole plant

(nmol CO2

plant)1 s)1) Ratio (%)†

Day 15

CNT (27 ⁄ 22) 10.6 25.2 42.1

HNT (27 ⁄ 27) 10.0 23.2 42.9

Day 30

CNT (27 ⁄ 22) 2.64 5.10 51.9

HNT (27 ⁄ 27) 0 13.9 0

†Ratio of respiration of the panicle to the whole plant. Values are means(n = 2).



grain weight under high night temperature conditions is

the result of events at the whole plant level. Morita et al.

(2004) pointed out the possibility of increased panicle

respiratory losses under high night temperature condi-

tions. Chowdhury and Wardlow (1978) reported a

decline in grain weight with increased seed respiratory

losses at high temperatures in cereals including wheat,

barley and sorghum. However, our results clearly indicate

that panicle respiration decreased to almost zero just after

the early cessation of grain development (Table 3). This

indicates that a decline in grain weight at high night tem-

perature is not caused by panicle respiratory losses.

Our results indicated that the final total biomass at the

harvest stages did not differ between the treatments

(Fig. 1). These results suggest that the decline in yield at

high night temperature was not caused by a promotion of

respiratory loss. Similarly, Morita et al. (2004) observed

no correlation between grain weight and whole plant

biomass under varying day ⁄ night temperatures, and

considered that the decline in grain weight at high temper-

ature was not caused by a carbohydrate deficit in sources

as a result of increased respiration loss. We found greater

accumulation of starch in the stems in the high night

temperature treatment just after the cessation of grain

development (Fig. 3), and net CO2 uptake per day tended

to be higher in this treatment (Table 2). In addition, the

starch content decreased after the cessation of grain devel-

opment (Fig. 3) and the dry weight of other plant parts,

including dead organs and new tillers, was greater at the

final stages (Fig. 1). From these results, we consider the

possibility that a decline in yield at high night temperature

is the result of changes in carbon allocation to new sinks

for vegetative reproduction at the whole plant level. How-

ever, we cannot rule out another possibility that an early

cessation of grain development by high night temperature

gives rise to carbon reallocation to new tillers. In fact,

Nakano et al. (1995) observed that trimming of the pani-

cles stimulates the development of late tillers and roots. In

their experiments, the photosynthate after trimming of the

panicles was efficiently translocated to other organs, such

as new tillers and roots. Similar results were observed by

Sato and Takahashi (1971) in rice growing under different

day ⁄ night temperatures. Thus, further experiments are

needed to determine changes in source and sink regulation

under high night temperature conditions.

Rice yield is always higher in northern Japan than in

southern Japan (Murata 1964). Our results clearly indi-

cate that a cool night temperature tends to favor carbon

allocation to panicles, resulting in higher yield. The rice

cultivar Oryza sativa originates from Asian wild strains of

Oryza rupifigon, with continuous variation between the

annual and perennial types (for a review see Morishita

1984). Therefore, perenniality associated with the ances-

tral species may have a strong influence on the enormous

diversity of O. sativa. As O. sativa can ratoon, individu-

als are essentially perennial (Oka and Morishita 1967).

Previously, Sano and Morishita (1982) highlighted that

O. sativa shows higher reproductive (annual) effort in

suboptimal environments than in optimal environments.

Thus, under high night temperature conditions individuals

may partially switch from an annual form to a perennial

form because rice is a tropical plant.

ACKNOWLEDGMENTS

This work was supported by a grant from the Ministry

of Agriculture, Forestry and Fisheries of Japan (Genomics

for Agricultural Innovation, GPN-0007), Scientific

Research B from the Japan Society for the Promotion of

Science (No. 20380041) and Research in a Proposed

Research Area (Planned Research No. 21114006) from

the Ministry of Education, Culture, Sports, Science and

Technology. We wish to thank Professor Emeritus Tada-

hiko Mae for his valuable advice and comments during

the course of this study. We also thank Professors Yukio

Watanabe and Hikaru Goto for their encouragement on

this work and Dr Louis J. Irving for critical reading of the

manuscript.

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increased grain yield and biomass allocation in rice under cool night temperature

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