Review

Tansley review
Blackwell Publishing Ltd

Grain filling of cereals under soil drying

Author for correspondence: Jianchang Yang1 and Jianhua Zhang2

Jianhua Zhang 1
Key Laboratory of Crop Genetics and Physiology of Jiangsu Province, Yangzhou University, Yangzhou,
Tel: +852 34117350
Fax: +852 34115995 Jiangsu, China; 2Department of Biology, Hong Kong Baptist University, Hong Kong, China
Email: jzhang@hkbu.edu.hk
Received: 23 June 2005
Accepted: 18 September 2005

Contents

Summary 223 IV. Hormonal regulation of whole-plant senescence

and grain filling 229
I. Introduction 224
V. Activities of key enzymes involved in carbon
II. Problems in grain filling: unfavorably delayed remobilization and grain filling 230
whole-plant senescence 224
VI. Conclusions 232
III. Controlled soil drying improves carbon remobilization
and grain filling as a result of enhanced whole-plant Acknowledgements 232
senescence 225
References 232

Summary

Key words: carbon reserve, cereals, grain
filling, remobilization, senescence, soil
drying, water stress.
Monocarpic plants require the initiation of whole-plant senescence to remobilize
and transfer assimilates pre-stored in vegetative tissues to grains. Delayed whole-
plant senescence caused by either heavy use of nitrogen fertilizer or adoption of
lodging-resistant cultivars/hybrids that remain green when the grains are due to
ripen results in a low harvest index with much nonstructural carbohydrate (NSC)
left in the straw. Usually, water stress during the grain-filling period induces early
senescence, reduces photosynthesis, and shortens the grain-filling period; however, it
increases the remobilization of NSC from the vegetative tissues to the grain. If mild soil
drying is properly controlled during the later grain-filling period in rice (Oryza sativa)
and wheat (Triticum aestivum), it can enhance whole-plant senescence, lead to
faster and better remobilization of carbon from vegetative tissues to grains, and
accelerate the grain-filling rate. In cases where plant senescence is unfavorably
delayed, such as by heavy use of nitrogen and the introduction of hybrids with
strong heterosis, the gain from the enhanced remobilization and accelerated grain-
filling rate can outweigh the loss of reduced photosynthesis and the shortened
grain-filling period, leading to an increased grain yield, better harvest index and
higher water-use efficiency.

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I. Introduction
Grain filling is the final stage of growth in cereals where
fertilized ovaries develop into caryopses. Its duration and rate
determine the final grain weight, a key component of the
total yield. In today’s crop production systems with their high
yield outputs, improvement in grain filling has become more
challenging than ever (Venkateswarlu & Visperas, 1987; Saini
& Westgate, 2000; Zahedi & Jenner, 2003).
Grain filling in cereals depends on carbon from two
resources: current assimilates transferred directly to the grain
and assimilates redistributed from reserve pools in vegetative
tissues either pre- or post-anthesis (Pheloung & Siddique, 1991;
Kobata et al., 1992; Schnyder, 1993). Reserve pools provide
the substrate needed to maintain transport and supply of
assimilate to grains during the dark period of the diurnal cycle
and during the later grain-filling period, when the photosynthetic
apparatus is senescing and the rate of dry matter accumu-
lation of grains exceeds the rate of dry matter accumulation of
the total crop (Schnyder, 1993). Under adequate moisture
conditions, pre-anthesis assimilate reserves in the stems and
sheaths of wheat (Triticum aestivum) and rice (Oryza sativa)
contribute 10–40% of the final grain weight (Rawson &
Evans, 1971; Gallagher et al., 1976; Bidinger et al., 1977;
Schnyder, 1993; Gebbing & Schnyder, 1999). Remobilization
of reserves to the grain is critical for grain yield if the plants are
subjected to water stress (unfavorable to the point of being
stressful) or if the yield potential is largely based on high
biomass accumulation (Yoshida, 1972; Nicolas et al., 1985a,b;
Palta et al., 1994; Ehdaie & Waines, 1996; Asseng & van Her-
waarden, 2003; Plaut et al., 2004).
It is generally believed that the process of grain filling is
regulated either genetically or environmentally (Yoshida, 1972;
Venkateswarlu & Visperas, 1987; Saini & Westgate, 2000). In
rice, most indica cultivars usually exhibit a faster grain filling
rate than japonica cultivars (Zhu et al., 1997; Cao et al., 1992).
The hybrid of japonica/indica rice usually shows a slower
grain filling rate than other hybrid rice varieties, for example
the indica/indica hybrids (Yuan, 1994, 1998; Peng et al., 1999,
2003). Environmental disturbances also have a great influence
on grain filling. The sedentary nature of plants exposes them
constantly to variations in environmental conditions (Saini
& Westgate, 2000). Water or drought stress is one of the most
important factors limiting crop yields world-wide ( Jones &
Corlett, 1992; Beltrano et al., 1999; Boyer & Westgate, 2004).
Water stress occurring during early grain development curtails
the kernel sink potential by reducing the number of endosperm
cells and amyloplasts formed (Nicolas et al., 1985a; Ober et al.,
1991; Saini & Westgate, 2000), thus reducing grain weight
as a result of a reduction in the capacity of the endosperm
to accumulate starch, in terms of both rate and duration
(Yoshida, 1972; Brocklehurst, 1977; Nicolas et al., 1985b).
Recently it has been proposed that grain filling is closely
linked to the whole-plant senescence process (Zhang et al.,
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1998; Yang et al., 2000b; Mi et al., 2002). Unfavorably delayed
senescence, which in practice can be induced by either heavy
use of nitrogen (N) fertilizer or adoption of lodging-resistant
cultivars that stay ‘green’ for too long (i.e. plants remain green
when grains are due to ripen), results in a low grain-filling
rate, leading to many poorly filled grains. Usually, water stress
at grain filling induces early senescence and shortens the grain-
filling period but increases remobilization of assimilates from
the straw to the grains (Cock & Yoshida, 1972; Yoshida, 1972;
Kobata & Takami, 1981; Nicolas et al., 1985b; Palta et al.,
1994; Ehdaie & Waines, 1996; Asseng & van Herwaarden,
2003; Plaut et al., 2004). Soil drying is unfavorable to plant
growth but may not be unfavourable to the point of producing
stress. The question arises as to whether it is possible to take
advantage of soil drying-induced whole-plant senescence and
better carbon remobilization to improve grain yield in situa-
tions where slow grain filling, as a result of delayed senescence,
is a problem. Research relate to this question is the focus of
this review. The discussions here will cover:
• problems in grain filling and the relationship between
whole-plant senescence and carbon remobilization;
• the possibility that controlled soil drying during grain
filling induces whole-plant senescence and thereby enhances
carbon remobilization and grain filling;
• hormonal regulation of whole-plant senescence and grain
filling;
• enzymatic activity during carbohydrate remobilization and
grain filling.
II. Problems in grain filling: unfavorably delayed
whole-plant senescence
Remobilization and transfer of assimilates stored in vegetative
tissues to the grain in monocarpic plants such as rice and
wheat require the initiation of whole-plant senescence. Delayed
whole-plant senescence, which leads to poorly filled grains
and unused carbohydrate in straw, is a new problem increasingly
recognized in rice and wheat production in recent years. Slow
grain filling is almost always associated with delayed whole-
plant senescence (Mi et al., 2002; Gong et al., 2005). Although
farmers can choose cultivars with early maturation, there are
still situations in which delayed senescence is a serious problem
requiring attention.
(1) Heavy use of N fertilizers is well known to lead to delayed
senescence and, in the worst cases, canopy lodging. Although
farmers are generally aware of this, the problem still occurs
every year in some countries, especially in highly productive
areas (e.g. Yue, 1997; Dobermann et al., 2002; Buresh et al.,
2004). This is possibly related to the intensive nature of
agriculture today, with less arable land being used to feed
increasing numbers of people.
(2) The First Green Revolution made a breakthrough in wheat
and rice breeding for semidwarf cultivars that are lodging-
resistant and can accommodate more chemical fertilizers and

produce higher grain yields (Berry et al., 2004). Selection of
lodging-resistant cultivars, however, has led to another prob-
lem in some cases, namely that stems are short and strong but
stored nonstructural carbohydrate (NSC) is poorly used because
the plants may remain green when the grains are due to ripen,
particularly in the cases of some short-grain rice cultivars
(Yuan, 1994, 1998; Zhu et al., 1997). If weather conditions
are favorable, and if senescence is also ‘functionally’ delayed,
that is, photosynthesis and phloem translocation are func-
tional, such delayed senescence may help achieve higher dry
mass production and possibly higher grain yield (Thomas &
Smart, 1993). However, in many cases, kernels and their con-
necting rachis or rachilla seem to mature or senesce earlier
than the stem and leaves. Much unused NSC is left in the
stem and sheath as a result (e.g. Liang et al., 1994; Ricciardi
& Stelluti, 1995; Yang et al., 2002a).
(3) Introduction of hybrid rice has been a fantastic success in
China since the 1970s and in other parts of Asia since the
1990s (Yuan, 1998; Virmani, 2003). Hybrid rice has a yield
advantage of more than 20% over conventional rice and
helped China to increase the annual grain yield 8.3 million
tons from 1976 to 1995 (Yuan, 1998). Utilization of even
stronger heterosis from a hybrid between the japonica and
indica subspecies (or ecotypes) of rice has, however, also
encountered the problem of delayed senescence. Many grains
are poorly filled or unfilled (Yang et al., 2002a; Peng et al.,
2003; Yuan, 2003). Such hybrid genotypes seem too vigorous
in terms of staying ‘young’, and produce high biomass with a
much lower harvest index. Hybrid wheat creates a similar
problem (Gong et al., 2005): biomass production was 40%
higher but grain yield only 15% higher compared with ordinary
wheat in a yield trial.
We may define the cases described above as ‘senescence
unfavorably delayed’, which means that no gain is obtainable
from the extended grain-filling period. We must distinguish
this situation from that found in favorable conditions, where
early senescence should be avoided because it reduces photo-
synthesis during the grain-filling period and therefore reduces
grain weight (e.g. Zhang et al., 1998; Plaut et al., 2004).
It should be noted that too much N fertilization is a prob-
lem in China that has led to the occurrence of unfavorably
delayed senescence in both wheat and rice. This is mainly a
Table 1 Comparison between wheat (Triticum aestivum) plots that were well watered or unwatered during the grain-filling stage
Fate of fed 14C (14CO2 applied 10 d early)
Watering Time from anthesis
treatment to maturation (d) % in kernels
Well watered 41 41.3
Unwatered 31 81.3
The fate of fed 14C was measured on day 18 from anthesis.
The data are taken from Zhang et al. (1998).
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Tansley review Review 225
result of the intensive nature of China’s crop production
and government-subsidized prices of chemical fertilizers. In
Europe and other more developed areas, however, this may
not be a problem. Use of chemical fertilizers has very much
stabilized over the last few decades (e.g. Peng et al., 1999).
Delayed senescence in situations (2) and (3) described
above is basically a genetically controlled character and there
are no practical measures that can be taken to deal with this
problem. However, it is possible that lodging-resistant varieties
may be given more N fertilizer which may cause the canopy
to live longer. In northern Europe, where wheat lodging is a
serious problem, lodging-prone varieties can be expected to
senesce later than lodging-resistant varieties 7(Berry et al., 2004).
Situation (1) is managed in practice with so-called ‘appropriate
control of N fertilizers and canopy density’, which is often
carried out too late when crops are in the grain-filling stage. In
all of these three situations, slow grain filling is a yield-limiting
factor, and any way in which the rate of grain filling can be
enhanced should be beneficial to the final yield formation.
III. Controlled soil drying to improve carbon
remobilization and grain filling as a result of
enhanced whole-plant senescence
Our experience with field-grown wheat has indicated that soil
drying during the grain-filling period can greatly enhance
early senescence (Table 1). The grain-filling period was shortened
by 10 d (from 41 to 31 d) in unwatered (during the grain-
filling period) plots, but a faster grain-filling rate and enhanced
remobilization of pre-stored carbohydrate were achieved
(Table 1). It seems possible that controlled soil drying at the
later grain-filling stage may promote whole-plant senescence,
leading to increased re-translocation of the pre-stored carbon
reserve in the stem and sheath.
The mechanisms by which the utilization of pre-stored
assimilates was enhanced are not known. Many processes are
likely to be involved, including the hydrolysis of stored carbo-
hydrate, phloem loading, long-distance translocation and
phloem unloading into the kernels. Whatever the mecha-
nisms may be, it is of interest to determine whether such a
treatment (i.e. soil drying) can be beneficial to grain filling
in cases where grain filling is slow, apparently as a result of
Total sugars left in stem (%)
% in stem (day 26 from anthesis)
40.5 29
9.6 8
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delayed senescence. The rationale behind such an approach is

as follows.
(1) Mild soil drying may not seriously disrupt phloem func-
tion. It has been shown that phloem translocation may be
less susceptible to drought than leaf photosynthesis (Boyer
& McPherson, 1975; Kozlowski, 1978).
(2) The period during which a developing grain receives
assimilates, that is the filling period, may be limited by the
life-span of its phloem link. Faster filling will certainly have
some advantages if the season is limited. It has been shown
that ‘stay-green’ (or delayed senescence) is not necessarily
associated with the full function of photosynthesis ( Thomas
& Smart, 1993). It is also possible that the phloem link to the
grains may lose its function before chlorophyll disappears
from the leaves of ‘stay-green’ genotypes.
(3) Even in weather conditions that may permit delayed
senescence to produce increased photosynthetic assimilation
(e.g. in the functionally ‘stay-green’ varieties), the gain from
accelerated grain filling from the pre-anthesis carbon reserve
may outweigh any loss of photosynthesis as a result of imposed
soil drying. Some delayed senescence seems to be genetically
controlled, for example in lodging-resistant cultivars that stay
green too long or in hybrid cultivars with heterosis that is too
strong. These cultivars always leave a substantial amount
(200–280 g m−2) of NSC unused in their straw. It has been
shown in maize (Zea mays) that it is the fast reallocation of
stem carbohydrate that is responsible for the high grain weight,
rather than the ‘stay-green’ characteristics (Dwyer et al., 1995). Fig. 1 Changes in leaf water potentials of rice, Oryza sativa (cv.
Here, the term ‘controlled soil drying’ refers to situations in Wuyujing 3) (a) and wheat, Triticum aestivum (cv. Yangmai 158)
(b) during the first 30 d (a) or 24 d (b) after withholding water.
which crops are not soil-dried to such an extent that overnight Treatments were normal amounts of nitrogen (NN) + well watered
rehydration cannot be completed and photosynthesis is (WW); high amounts of nitrogen (HN) + WW; NN + soil drying (SD);
severely inhibited. It should be stressed that the soil drying and HN + SD. Measurements were made on the flag leaves predawn
should be at the later stage of grain filling because the early (PD, 06:00 h) and at midday (MD, 11:30 h). Vertical bars represent
development of the embryo (at the rapid cell division stage), ± the standard error of the mean (n = 6) where they exceed the size
of the symbol. Data are adapted from Yang et al. (2001d, 2004a).
that is the ‘grain-setting’ stage, is very susceptible to water stress
(Nicolas et al., 1985a; Boyle et al., 1991; Saini & Westgate,
2000; Boyer & Westgate, 2004). Severe water stress immediately
after fertilization can cause serious abortion of kernel develop-
ment in maize (Boyle et al., 1991) and spikelet sterility in rice grain-filling periods of rice and wheat is controlled properly
(Ekanayake et al., 1989, 1993). so that plants can rehydrate overnight (i.e. the predawn leaf
It should be noted that wheat grain yield is more vulnerable water potential is not statistically different from that of well-
to a shortened grain-filling period than rice grain yield. In watered plants), photosynthesis should not be severely inhibited
wheat, grain size can be greatly decreased by reduced irrigation (Figs 1 and 2). One benefit of such soil drying is that it can
during grain filling (Zhang et al., 1998). However, in cases enhance plant senescence and lead to faster and better remo-
where stay-green is a problem as a result of heavy use of N, bilization of pre-stored carbon from vegetative tissues to the
moderate soil drying may not necessarily reduce the grain grains (Table 2). The early senescence induced by soil drying
yield of wheat (see discussion in section III). does not necessarily reduce the grain yield (on a dry weight
In field experiments with highly lodging-resistant cultivars basis) even when the plants are grown under normal N
(total precipitation, mean solar radiation and daily tempera- conditions. Furthermore, in cases where plant senescence is
ture during the grain-filling period were 105 and 142 mm, unfavorably delayed, such as by heavy use of N, the gain from the
16.8 and 18.4 MJ m−2 d−1, and 19.2 and 24.8°C, respectively, enhanced remobilization and accelerated grain-filling rate
for wheat and rice), our results (Yang et al., 2000b, 2001b,c,d, may outweigh the loss of photosynthesis and the shortened
2004a) showed that, if soil drying (soil water potential of grain-filling period and increase the grain yield and harvest
− 0.05 MPa for rice and −0.08 MPa for wheat) during the index (Table 3).

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Table 2 Remobilization of pre-stored assimilates in the straw of rice, Oryza sativa (cv. Wuyujing 3) and wheat, Triticum aestivum (cv. Yanfu
188) subjected to various nitrogen and soil moisture treatments

Water Nitrogen Remobilized carbon Contribution to NSC in residue Total dry Harvest
Crop treatment applied reserve (%) grain (%) (mg g−1 d. wt) matter (g m−2) index

Rice WW NN 48 c 14 c 142 b 1707 a 0.47 c

WW HN 25 d 7.6 d 219 a 1741 a 0.41 d
SD NN 75 a 29 a 65 d 1538 b 0.52 a
SD HN 61 b 22 b 104 c 1717 a 0.50 b
Wheat WW NN 57 c 23 c 134 b 1764 a 0.42 c
WW HN 33 d 22 c 231 a 1503 b 0.38 d
SD NN 79 a 44 a 67 d 1477 b 0.44 a
SD HN 65 b 36 b 112 c 1714 a 0.43 b

The cultivars used were highly lodging-resistant, that is they stay green when grains are mature.
NN and HN indicate normal and high amounts of nitrogen application at heading time, respectively. WW and SD indicate the well-watered and
soil-drying treatments during the grain-filling period, respectively. Values are means of 20 plants. Different letters indicate statistical significance
at P < 0.05 within a column and within the same crop. NSC, nonstructural carbohydrate in straw; d. wt, dry weight.
Data are taken from Yang et al. (2000b, 2001d).

When senescence is unfavorably delayed, rice and wheat will

Fig. 2 Photosynthetic rates in the flag leaves of rice, Oryza sativa
(cv. Wuyujing 3) (a) and wheat, Triticum aestivum (cv. Yufu 188)
(b) during the grain-filling period. Treatments were normal amounts
of nitrogen (NN) + well watered (WW); high amounts of nitrogen (HN)
+ WW; NN + soil drying (SD); and HN + SD. Arrows indicate the start
of the period in which water was withheld. Vertical bars represent ±
the standard error of the mean (n = 6) where they exceed the size of
the symbol. Data are adapted from Yang et al. (2000b, 2001d).
show prolonged, slow grain filling, for example under high-N
conditions (Fig. 3). Controlled soil drying increases grain-
filling rates and shortens grain-filling periods. The increased rate
and the shortened period are especially remarkable in high-N
conditions (Figs 3c,d). Our results (Yang et al., 2001d, 2003c,
2004a) with lodging-resistant cultivars also showed that the
final grain weight was not significantly different between well-
watered and soil-drying treatments when a normal amount of
N was applied. However, it was significantly increased under
soil drying plus high-N treatment, implying that the gain
from accelerated grain-filling rate outweighed the possible loss
of photosynthesis as a result of a shortened grain-filling period
when plants were subjected to soil drying during grain filling.
The hybrid of japonica/indica rice possesses stronger heter-
osis in biomass production than other hybrid rice varieties, for
example the currently used indica/indica hybrid rice (Yuan,
1994, 2003; Peng et al., 1999, 2003). Too many poorly filled
grains, however, hinder the exploitation of such heterosis
(Yuan, 1994, 1998), and have been attributed to many factors
(e.g. Yuan, 1994, 1998; Peng et al., 1999, 2003; Yang et al.,
2002a). The slow grain filling that results from delayed whole-
plant senescence is considered the main cause of poor grain
filling (Yuan, 1994, 1998; Zhu et al., 1997; Peng et al., 1999,
2003; Yang et al., 2002a). Controlled soil drying imposed
during grain filling substantially enhanced the remobilization
of pre-stored carbohydrate (98–124 g m−2) to the grains,
accelerated the grain-filling rate, and increased the grain
yield of japonica/indica hybrids (Yang et al., 2002c). Similar
findings were obtained in two-line hybrid rice that shows slow
grain filling mainly as a result of delayed senescence (Yang
et al., 2003a). Moderate soil drying imposed during the grain-
filling period substantially accelerated the grain-filling rate.
The grain weight and grain yield were actually improved, rather
than reduced, by the moderate soil drying (Table 4).

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Table 3 Grain-filling rate and grain yield of rice, Oryza sativa (cv. Wuyujing 3) and wheat, Triticum aestivum (cv. Yangmai 158) subjected to
various nitrogen and soil moisture treatments

Active Total number of

Water Nitrogen grain-filling Grain-filling rate spikelets/grains Ripened Grain weight Grain yield
Crop treatment applied period (d) (mg d−1 per grain) × 103 m−2 grain (%) (mg per grain) (g m−2)

Rice WW NN 20 b 1.21 c 33.73 a 90.8 b 26 b 802 b

WW HN 25 a 0.91 d 33.78 a 84.2 c 25 c 714 c
SD NN 17 c 1.39 a 33.71 a 90.2 b 26 b 780 b
SD HN 19 b 1.28 b 33.62 a 94.2 a 27 a 858 a
Wheat WW NN 27 b 1.40 c 17.18 a – 42 b 701 b
WW HN 34 a 0.95 d 17.81 a – 36 c 628 c
SD NN 19 d 1.94 a 16.68 a – 41 b 679 b
SD HN 24 c 1.69 b 17.90 a – 45 a 785 a

The cultivars used were highly lodging-resistant, that is they stay green when grains are mature.
NN and HN indicate normal and high amounts of nitrogen application at heading time, respectively. WW and SD indicate well-watered and
soil-drying treatments during the grain-filling period, respectively. The active grain-filling period and grain filling were calculated according to
the Richards (1959) equation. Values for total number of spikelets or grains, grain weight and percentage of ripened grains were means of plants
harvested from 2 m2 of each treatment. The grain yield was the mean from 15–18 m2 of each treatment and was calculated on a dry weight
basis. Different letters indicate statistical significance at P < 0.05 within a column and within the same crop.
Data are taken from Yang et al. (2001d, 2004a).

Fig. 3 The grain-filling process (a, b) and grain-filling rate (c, d) of rice, Oryza sativa (cv. Wuyujing 3) (a, c) and wheat, Triticum aestivum
(cv. Yangmai 158) (b, d) subjected to various nitrogen and soil moisture treatments. Treatments were normal amounts of nitrogen (NN) + well
watered (WW); high amounts of nitrogen (HN) + WW; NN + soil drying (SD); and HN + SD. Grain-filling rate was calculated according to the
Richards (1959) equation. Arrows indicate the start of the period in which water was withheld. Vertical bars in (a) and (b) represent ± the
standard error of the mean (n = 3) where they exceed the size of the symbol. Data are adapted from Yang et al. (2001c, 2004a).

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Table 4 Grain-filling rate and grain yield of rice (Oryza sativa) subjected to various soil moisture treatments

Water deficit Active grain-filling Grain-filling rate Total number of Ripened Grain weight Grain yield
Hybrid treatment period (d) (mg d−1 per grain) spikelets × 103 m−2 grain (%) (mg per grain) (g m−2)

Pei-Ai 64S/Yangdao 6 WW 44 a 0.52 c 52.9 a 73.4 b 25.6 b 994 b

MD 39 b 0.61 b 51.7 a 77.8 a 26.8 a 1077 a
SD 32 c 0.71 a 51.9 a 72.6 b 25.2 b 949 b
Pei-Ai 64S/E32 WW 46 a 0.49 c 49.9 a 70.2 b 25.3 b 886 b
MD 40 b 0.59 b 49.1 a 74.1 a 26.4 a 959 a
SD 33 c 0.68 a 49.8 a 69.7 b 24.9 b 863 b

Two two-line indica hybrids Pei-Ai 64S/Yangdao 6 and Pei-Ai 64S/E 32 were field grown. WW, MD and SD indicate well-watered conditions,
moderate soil drying and severe soil drying, respectively, during grain filling. The active grain-filling period and grain-filling rate were calculated
according to the Richards (1959) equation. The total number of spikelets, the percentage of ripe grains, and grain weight were means of plants
harvested from 3 m2 of each treatment. Grain yield was the mean of plants harvested from 12 m2 of each treatment and was calculated on a
dry weight basis. Different letters indicate statistical significance at P < 0.05 within a column and within the same hybrid.
Data are taken from Yang et al. (2003a).

In theory, N metabolism and respiration should affect grain
filling (Ntanos & Koutroubas, 2002). However, information
linking N/protein metabolism and respiration under soil dry-
ing to grain filling is lacking in the literature. It is possible that
soil N availability is reduced under soil drying and N uptake
is curtailed. Advancing senescence may therefore inhibit
canopy protein remobilization, reduce grain protein synthesis,
and hence increase yield by a reduction in respiratory require-
ment. This possibility is worthy of investigation.
IV. Hormonal regulation of whole-plant
senescence and grain filling
Extensive studies have demonstrated that post-anthesis water
deficits result in early senescence and more remobilization of
pre-anthesis stored assimilates to grains in cereals (Gallagher
et al., 1976; Johnson & Moss, 1976; Jones & Rawson, 1979;
Austin et al., 1980; Lauer & Simmons, 1985; Nicolas et al.,
1985b; Kobata et al., 1992; Palta et al., 1994; Zhang et al.,
1998). However, the mechanisms by which plant senescence
promotes remobilization of assimilates are rather obscure.
Very little is known about the relationship between these two
processes, a surprisingly neglected subject given its importance
to yield formation.
Many factors, either endogenous or environmental,
contribute to plant senescence (Nooden, 1988a; Smart, 1994;
Lers et al., 1998; Pic et al., 2002), but abscisic acid (ABA)
and cytokinins are generally believed to be two of the major
regulators of plant senescence ( Biswas & Choudhuri, 1980;
Nooden, 1988b; Zeevaart & Creelman, 1988; Haberer &
Kieber, 2002). High concentrations of cytokinins in plants
can delay senescence (Buchanan-Wollaston, 1997), whereas a
high ABA concentration has the opposite effect (Nooden,
1988b; Madhu et al., 1999; Tadas et al., 1999). ABA also has
been reported as an important regulator in the transport of
assimilates to the developing seeds or fruits (Dewdney &
McWha, 1979; Tietz et al., 1981; Clifford et al., 1986;
Brenner & Cheikh, 1995). However, contradictory data on the
involvement of ABA in the regulation of both senescence and
assimilate remobilization have been reported (Setter et al.,
1980; Nooden, 1988a; Barratt et al., 1989; Ober & Setter,
1990; Brown et al., 1991; de Bruijn & Vreugdenhil, 1992).
Our work (Yang et al., 2001b, 2002d, 2003d) on both rice
and wheat demonstrated that the remobilization of pre-stored
assimilates was closely associated to whole-plant senescence.
Soil drying during the grain-filling period enhanced senes-
cence and led to more and faster remobilization of pre-stored
carbon assimilates from the stems to grains. In contrast, heavy
use of N slowed senescence and retarded such remobilization.
Such results indicate that senescence and remobilization are
coupled processes in rice and wheat. Our results (Yang et al.,
2002d, 2003d) showed that soil drying substantially increased
ABA accumulation (concentration) in the leaves and stems or
root exudates, and markedly reduced cytokinins (zeatin and
zeatin riboside) in the leaves. ABA was significantly and
negatively correlated with the photosynthetic rate and chloro-
phyll content of the flag leaves, while cytokinins were positively
correlated with these variables. Spraying 20 × 10−6 M ABA
significantly reduced the chlorophyll content, whereas spray-
ing 40 × 10−6 M kinetin increased it. These results suggest that
both ABA and cytokinins are involved in controlling senes-
cence in rice and wheat under conditions of soil drying.
We observed that elevated ABA concentrations in the stems
or root exudates were associated with the partitioning of pre-
feed 14C in the grains in soil drying treatments. ABA in both
the leaves and stems, but not cytokinins, was significantly and
positively correlated with remobilization of pre-stored carbon,
and such remobilization was enhanced by exogenous ABA,
suggesting that enhanced remobilization by soil drying during
grain filling can be attributed, at least partly, to an elevated
ABA concentration in the plant.
It is well known that plant hormones are involved in grain
filling and seed development (e.g. Davies, 1987; Brenner
& Cheikh, 1995; Yang et al., 2000a, 2002b, 2003b). There are

© The Authors (2005). Journal compilation © New Phytologist (2005) www.newphytologist.org New Phytologist (2006) 169: 223– 236
230 Review Tansley review
Table 5 Correlation coefficients between hormone concentrations/ratios in the grains and grain-filling rates during the active grain-filling period
(the linear increase period for grain dry weight) of rice (Oryza sativa)
Hormone concentration/ratio Coefficients
Cytokinins (CK) 0.69*
Indole-3-acetic acid (IAA) 0.46, 0.42
Gibberellins (GAs) 0.38, − 0.14
Abscisic acid (ABA) 0.95**, 0.98**, 0.74**
Ethylene (Ethy) − 0.78**
CK:IAA 0.37
CK:GAs 0.52
IAA:GAs 0.45
Ethy:ABA 0.79**
GAs:ABA 0.63*
Data are taken from the references listed in the table. *, ** indicate statistical significance at the P < 0.05 and P < 0.01 levels, respectively.
many reports of auxins, gibberellins (GAs) and ABA regulat-
ing grain development (Karssen, 1982; Davies, 1987; Kende
& Zeevaart, 1997). In rice grains, hormone content (per grain)
and hormone concentration (per unit weight) are significantly
correlated, and both vary with grain-filling stage (Yang et al.,
2000a). We (Yang et al., 2001c) observed that cytokinins and
indole-3-acetic acid contents in rice grains transiently increased
at the early filling stage and coincided with the rapid increase
in grain-filling rate. The heights and timings of such peaks
were regulated by N nutrition status, with high N being asso-
ciated with lower peaks and their later appearance. Controlled
soil drying only hastened declines in cytokinins and indole-3-
acetic acid contents at the late grain-filling stage.
Contents of GAs (GA1 + GA4) in rice grains were also
higher at the early grain-filling stage than at the late stage.
High N enhanced, while soil drying substantially reduced,
GA accumulation. ABA content in the rice grains was low at
the early grain-filling stage, reaching a maximum when the
grain-filling rate was highest. Soil drying greatly increased
ABA accumulation in the grains. The peak values of ABA in
the grains were significantly correlated with the maximum
grain-filling rates. Our results (Yang et al., 2001c) suggest that
an altered hormonal balance in the grains produced by soil
drying during grain filling, especially a decrease in GAs and an
increase in ABA, enhances the remobilization of pre-stored
carbon to the grains and accelerates the grain-filling rate.
It was reported that an antagonistic relationship between
ABA and ethylene mediates root and shoot growth in maize
(Spollen et al., 2000) and tomato (Lycopersicon esculentum)
(Hussain et al., 2000; Sharp et al., 2000; Sharp, 2002) when
plants are subjected to water stress. We observed that, in con-
trast to that of ABA, the concentration (evolution rate) of
ethylene in rice grains was very high at the early grain-filling
stage and sharply decreased during the linear period of grain
growth (Yang et al., 2004c). Moderate soil drying reduced,
whereas severe soil drying increased, ethylene accumulation.
The ethylene concentration was significantly and negatively
correlated with the grain-filling rate. Application of cobalt
New Phytologist (2006) 169: 223– 236 www.newphytologist.org © The Authors (2005). Journal compilation © New Phytologist (2005)
References
Yang et al. (2000a)
Yang et al. (2000a, 2001c)
Yang et al. (2000a, 2001c)
Yang et al. (2001c, 2003b, 2004c)
Yang et al. (2004c)
Yang et al. (2000a)
Yang et al. (2000a)
Yang et al. (2000a)
Yang et al. (2004c)
Yang et al. (2001c)
ion (an inhibitor of ethylene synthesis) or ABA at the early
grain-filling stage significantly increased the grain-filling rate.
Spraying with ethephon (an ethylene-releasing agent) or flu-
ridone (an inhibitor of ABA synthesis) had the opposite effect
(Yang et al., 2004c). The results indicate that the effect of ABA
and ethylene on grain-filling rate depends not only on their
concentrations but also on their balance. Correlation coefficients
between hormone concentrations/ratios and grain-filling
rate based on the hormone measurements we have made in
various studies are listed in Table 5.
V. Activities of key enzymes involved in carbon
remobilization and grain filling
The main storage form of NSC in the stem (culm + sheath) of
rice is starch (Murayama et al., 1961; Murata & Matsushima,
1975; Cao et al., 1992). Starch needs to be degraded as glucose
first and then sucrose is re-synthesized when the carbon
is remobilized from the stem to the grains (Murayama
et al., 1961; Venkateswarlu & Visperas, 1987; Beck & Ziegler,
1989). Starch degradation can occur via hydrolytic and
phosphorolytic reactions, or probably the concerted action of
several enzymes (Beck & Ziegler, 1989; Nielsen et al., 1997).
These enzymes are likely to include α-amylase, β-amylase,
α-glucosidase, and starch phosphorylase. Based on its high
affinity, sucrose-phosphate synthase (SPS) is expected to
play a major role in the re-synthesis of sucrose (Whittingham
et al., 1979; Wardlaw & Willenbrink, 1994) and sustain the
assimilatory carbon flux from source to sink (Isopp et al.,
2000). There are reports that starch degradation in stolons of
white clover is controlled by α-amylase activity (Gallagher
et al., 1997). Water stress can induce α-amylase in barley
leaves (Jacobsen et al., 1986) and enhance β-amylase activity
in cucumber cotyledons (Todaka et al., 2000). We ( Yang et al.,
2001a) also investigated all the possible enzymes involved in
starch degradation and sucrose re-synthesis in rice stems
during grain filling. Our results showed that both α- and
β-amylase activities were enhanced by soil drying, with the

former enhanced more than the latter, and significantly
correlated with the concentrations of soluble sugars in the
stems. The other two possible starch-breaking enzymes, α-
glocosidase and starch phosphorylase, showed no significant
differences in activities between the well-watered and water
stress treatments. Soil drying also increased the SPS activity
that is responsible for sucrose production. These results
suggest that the fast hydrolysis of starch and increased carbon
remobilization are attributable to enhanced α-amylase and
SPS activities in rice stems under soil drying.
In contrast to those in rice stems, the main storage forms
of water-soluble carbohydrates (WSCs) in wheat stems are
fructans and sucrose ( Judel & Mengel, 1982; Blacklow
et al., 1984; Hendrix et al., 1986; Kühbauch & Thome, 1989;
Wardlaw & Willenbrink, 1994; Yukawa et al., 1995). This
storage peaks well into the period of grain filling under adequate
moisture conditions and declines during the later stages of
kernel development to supply a high proportion of the assimilates
needed for concurrent kernel development (e.g. Wardlaw &
Willenbrink, 1994). At the stage of maximum WSC content,
fructans and sucrose represented 85% and 10%, respectively,
of the WSCs in wheat stem internodes (Blacklow et al.,
1984). The reserve of WSCs is likely to be determined by the
activity of enzymes associated with both fructan and sucrose
metabolism in the wheat stem. It has been reported that the
synthesis of high-molecular-weight fructan is catalyzed by
sucrose-sucrose fructosyl transferase (SST) and fructan-fructan
fructosyl transferase (Nelson & Spollen, 1987; Housley et al.,
1989; Pollock & Cairns, 1991). SST is considered to be the
most important enzyme for fructan synthesis as it increases
concomitantly with fructan accumulation (Wagner et al., 1986;
Dubois et al., 1990; Yukawa et al., 1995). Fructan exohydrolase
(FEH) catalyzes the hydrolysis of fructans, leading to the release
of fructose which, in turn, has to be converted to the precursors
required for the re-synthesis of sucrose, catalyzed by enzymes
involved in the synthesis of sucrose, mainly SPS (Huber &
Huber, 1996), before phloem loading (Simpson & Bonnett,
1993; Willienbrink et al., 1998). Our results (Yang et al., 2004b)
showed that both FEH and SPS activities were substantially
enhanced by controlled soil drying during the grain-filling
period and positively correlated with the total NSC and
fructan remobilization from wheat stems. The activity of
acid invertase, a hydrolase cleaving sucrose irreversibly into
glucose and fructose (Sturm & Tang, 1999; Wang et al.,
2000), was also enhanced by soil drying and associated with
the change in fructan concentration, but not correlated with
the total NSC remobilization and pre-feed 14C increase (indi-
cating fast filling) in the grains. SST activity was inhibited by
soil drying and negatively correlated with the remobilization
of carbon reserves. All of these results demonstrate that source-
supplying capacity is increased by regulation of key enzymes
involved in the hydrolysis of fructans and the synthesis of
sucrose when controlled soil drying accelerates carbon
remobilization.
© The Authors (2005). Journal compilation © New Phytologist (2005) www.newphytologist.org
Tansley review Review 231
On the sink side, grain filling is a process of active metab-
olism of carbohydrate and starch accumulation in kernels. It
is generally accepted that four enzymes may play a key role in
this process: sucrose synthase (SuSase), ADP glucose pyro-
phosphorylase (AGPase), starch synthase (StSase), and starch
branching enzyme (SBE) (Hawker & Jenner, 1993; Ahmadi
& Baker, 2001; Hurkman et al., 2003). SuSase catalyses the
cleavage of sucrose, the main transported form of assimilates
in wheat plants (Fisher & Gifford, 1986), to form UDP-glucose
and fructose, which is thought to be the first step in sucrose-
to-starch conversion. Its activity is considered to be linked to
sink strength in the developing rice grain and tomato fruit
(Sun et al., 1992; Wang et al., 1993; Kato, 1995). AGPase
produces ADP-glucose, the primer of the starch chain (Smith
& Denyer, 1992), and is regarded as the rate-limiting enzyme
in starch biosynthesis (Preiss, 1988). StSase, composed of both
soluble and granule-bound isoforms, elongates the amylose
and amylopectin chains (Déjardin et al., 1997). Soluble StSase
(SSS) activity is reported to be positively correlated with the
rate of starch synthesis in wheat grains (Keeling et al., 1993).
SBE forms branches on the polymers. It cleaves α-1,4 bonds
on both amylose and amylopectin molecules and reattaches
the released glucan segments to the same or another glucan
chain through the formation of α-1,6 linkages (Hurkman
et al., 2003). Its activity is closely associated with the increase
in starch content during the development of the rice endosperm
(Nakamura et al., 1989; Nakamura & Yuki, 1992).
Numerous studies have been performed on the effects of
heat stress on the activities of enzymes involved in sucrose-
to-starch metabolism in cereals (Caley et al., 1990; Hawker &
Jenner, 1993; Keeling et al., 1993; Jenner, 1994; Cheih &
Jones, 1995; Duke & Doehlert, 1996; Wilhelm et al., 1999;
Hurkman et al., 2003). A correlation of reduction in starch
content with declines in SuSase and SSS activities in heat-
treated grains has been reported in these studies. With the
exception of the work by Ahmadi & Baker (2001), who
reported that reduction in grain growth rate of water-stressed
wheat plants resulted from reduced SSS activity, whereas
growth cessation resulted mainly from the inactivation of
AGPase, information is scarce on changes in activities of
key enzymes in the sucrose-to-starch catalytic pathway in
water-stressed wheat and rice grains during the grain-filling
period.
In our studies of rice and wheat grain filling under controlled
soil drying (Yang et al., 2003c, 2004a), activities of SuSase,
SSS and SBE in the grains were substantially enhanced by soil
drying and positively correlated with the starch accumulation
rate (SAR) in grains. AGPase activity was also enhanced by
soil drying and correlated with SAR with a smaller coefficient.
Activities of granule-bound starch synthase and soluble and
insoluble acid invertase in the grains were less affected by soil
drying. These results indicate that increased grain filling rate
is mainly attributable to enhanced sink activity through regu-
lation of key enzymes involved in sucrose-to-starch conversion,
New Phytologist (2006) 169: 223– 236
232 Review Tansley review
especially SuSase, SSS and SBE, in rice and wheat grains when
subjected to mild soil drying during grain filling.
We (Yang et al., 2001a, 2003c, 2004a,b) found that
enhanced activities of SPS and FEH in stems and SuSase, SSS
and SBE in grains were closely associated with elevated ABA
concentrations in grains. Our spraying experiments (Yang
et al., 2001a, 2003c, 2004a,b) showed that application of
ABA to well-watered plants gave similar results to those
obtained by soil drying. Spraying with fluridone, an ABA syn-
thesis inhibitor, had the opposite effect. These results suggest
that ABA plays a vital role in the regulation of the key enzymes
involved in carbon remobilization and metabolism of carbo-
hydrate in grains, although exogenously applied ABA could
produce multiple effects such as stomatal closure, which leads
to a reduction in photosynthesis, and ABA above normal con-
centrations in the grains under severe water stress may have an
inverse effect on filling as a result of a shortened grain-filling
period.
VI. Conclusions
If soil drying during the grain-filling period of rice and wheat
is controlled properly so that plants can rehydrate overnight,
photosynthesis should not be severely inhibited. A benefit of
such soil drying is that it can enhance whole-plant senescence
and lead to faster and better remobilization of pre-stored
carbon from vegetative tissues to the grains. The gain from
enhanced remobilization and accelerated grain-filling rate
may outweigh the loss of photosynthesis and the shortened
grain-filling period and increase grain yield and harvest index
in cases where plant senescence is unfavorably delayed. This
practice has great significance for agriculture for several reasons.
First, seasons for crop production are limited by adverse
weather conditions in many parts of the world. Continental
hot, dry winds common in early June in the north and middle
of China can dehydrate wheat in 1 or 2 d before it matures,
while the cold front in late autumn abruptly marks the end
of the rice season in east Asia. Controlled soil drying may
accelerate whole-plant senescence so that the wheat and rice
plants can mature before the adverse conditions occur. Secondly,
the heavy use of N results in unfavorably delayed senescence
and slow grain filling, leading to low grain weight. Early
senescence induced by soil drying could increase the rate of
grain filling and improve grain weight in this case. Thirdly,
some lodging-resistant rice and wheat cultivars or hybrids
have a low harvest index and poor grain filling because the
plants remain ‘green’ when the grains are due to ripen and
poorly remobilize assimilates to the grains. Controlled soil
drying may induce these cultivars or hybrids to mobilize more
pre-stored assimilates to grains. In addition, controlled soil
drying may contribute to water saving in rice and wheat
production, which is urgently needed to develop sustainable
agriculture in many parts of the world where the rapid
depletion of water resources is threatening crop production.
New Phytologist (2006) 169: 223– 236 www.newphytologist.org © The Authors (2005). Journal compilation © New Phytologist (2005)
How can controlled soil drying be applied during the
grain-filling period, if needed? We applied soil drying in the
field experiment by giving the crop small amounts of water
and monitoring soil water potentials. In commercial produc-
tion, control of soil drying may be achieved by monitoring
leaf rolling and wilting of older leaves as a sign of plant water
stress and applying small amounts of irrigation at a time.
Plants develop sequential responses, and the older leaves
usually show wilting first under prolonged soil drying (Zhang
& Davies, 1989). In agriculture, better regulation of the use
of N fertilizers has also become an urgent issue. In areas such
as China where food demand is high and chemical fertilizers
are relatively cheap, over-application of N fertilizers may not
only lead to serious environmental problems, but also cause
reduced yield as a result of delayed senescence, as discussed
above. Such a problem may also have implications for plant
water use efficiency. Over-expanded leaf areas and delayed
senescence will result in plants consuming water resources
that could be used for other purposes. Water shortage has
become the most limiting factor in crop production in many
parts of the world (e.g. Zhang & Yang, 2004).
Acknowledgements
We gratefully acknowledge support from the Research Grant
Council of Hong Kong (RGC 2165/05M; RGC 2149/04M),
the Area of Excellence for Plant and Fungal Biotechnology in
the Chinese University of Hong Kong, the National Natural
Science Foundation of China (grant no. 30270778, 30370828),
and the State Key Project (grant no. 2004BA520A12-5).
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