Journal of Integrative Agriculture 2016, 15(12): 2677–2687

Available online at www.sciencedirect.com

ScienceDirect

REVIEW

The causes and impacts for heat stress in spring maize during
grain filling in the North China Plain - A review

TAO Zhi-qiang1, 2*, CHEN Yuan-quan1*, LI Chao3, ZOU Juan-xiu1, YAN Peng1, YUAN Shu-fen1, WU Xia1,
SUI Peng1

1
College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, P.R.China
2
Institute of Crop Science, Chinese Academy of Agricultural Sciences/Key Laboratory of Crop Physiology and Ecology, Ministry of
Agriculture, Beijing 100081, P.R.China
3
Wuqiao Experimental Station, China Agricultural University, Cangzhou 061800, P.R.China

Abstract
High-temperature stress (HTS) at the grain-filling stage in spring maize (Zea mays L.) is the main obstacle to increasing
productivity in the North China Plain (NCP). To solve this problem, the physiological mechanisms of HTS, and its causes
and impacts, must be understood. The HTS threshold of the duration and rate in grain filling, photosynthetic characteristics
(e.g., the thermal stability of thylakoid membrane, chlorophyll and electron transfer, photosynthetic carbon assimilation), water
status (e.g., leaf water potential, turgor and leaf relative water content) and signal transduction in maize are reviewed. The
HTS threshold for spring maize is highly desirable to be appraised to prevent damages by unfavorable temperatures during
grain filling in this region. HTS has negative impacts on maize photosynthesis by damaging the stability of the thylakoid
membrane structure and degrading chlorophyll, which reduces light energy absorption, transfer and photosynthetic carbon
assimilation. In addition, photosynthesis can be deleteriously affected due to inhibited root growth under HTS in which plants
decrease their water-absorbing capacity, leaf water potential, turgor, leaf relative water content, and stomatal conductance.
Inhibited photosynthesis decrease the supply of photosynthates to the grain, leading to falling of kernel weight and even
grain yield. However, maize does not respond passively to HTS. The plant transduces the abscisic acid (ABA) signal to
express heat shock proteins (HSPs), which are molecular chaperones that participate in protein refolding and degradation
caused by HTS. HSPs stabilize target protein configurations and indirectly improve thylakoid membrane structure stability,
light energy absorption and passing, electron transport, and fixed carbon assimilation, leading to improved photosynthesis.
ABA also induces stomatal closure to maintain a good water status for photosynthesis. Based on understanding of such
mechanisms, strategies for alleviating HTS at the grain-filling stage in spring maize are summarized. Eight strategies have
the potential to improve the ability of spring maize to avoid or tolerate HTS in this study, e.g., adjusting sowing date to avoid

Received 8 December, 2015 Accepted 25 April, 2016

TAO Zhi-qiang, Tel: +86-10-82107635, E-mail: taozhiqiang@
caas.cn, CHEN Yuan-quan, Tel: +86-10-62731163,
E-mail: rardc@163.com; Correspondence SUI Peng,
Tel/Fax: +86-10-62731163, E-mail: suipeng@cau.edu.cn
*
These authors contributed equally to this study.
© 2016, CAAS. Published by Elsevier Ltd. This is an open
access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/)
doi: 10.1016/S2095-3119(16)61409-0
2678 TAO Zhi-qiang et al. Journal of Integrative Agriculture 2016, 15(12): 2677–2687
HTS, breeding heat-tolerance varieties, and tillage methods, optimizing irrigation, heat acclimation, regulating chemicals,
nutritional management, and planting geometric design to tolerate HTS. Based on the single technology breakthrough, a com-
prehensive integrated technical system is needed to improve heat tolerance and increase the spring maize yield in the NCP.
Keywords: North China Plain, spring maize, grain filling, heat-tolerance, heat-avoidance, gas exchange, water status
1. Introduction
Food security is an eternal theme and a problem for agri-
cultural development as the global population increases
(Leitner et al. 2014). China will continue to face a severe
grain demand challenge, and the national grain production
capacity will need to be 5 500 billion kg to meet basic sub-
sistence by 2020 (Tao et al. 2016). Maize is the main cereal
crop accounting for the largest planting area and total yield
in China, and thus enhancing the maize yield per unit area will
play a major role in ensuring national food security. The North
China Plain (NCP), one of the main maize-producing areas
in China, contributes substantially to national food produc-
tion. Total food yield and maize yield in the NCP accounted
for 34.6 and 29.0% of the national production respectively
(National Bureau of Statistics of the People’s Republic of
China 2014). Nevertheless, a severe water shortage is a
big issue for agriculture in the NCP (Ma et al. 2015). Water
resources in this area only account for 7.6% of the total, and
the average per capita is only one-fifth that of the nation. The
main cropping system in this area is a winter wheat-summer
maize rotation system, and that is a high water-consumption
system. It is estimated that winter wheat consumes >70%
of the irrigation water in the NCP (Li et al. 2005). Therefore,
exploring the development of a new water-saving cropping
system to replace part of the high water-consuming cropping
system has attracted research interest in recent years and
could resolve the water crisis in this area.
The production potential of spring maize under optimum
photosynthetic, temperature and water conditions is superior
to that of summer maize (Zhao et al. 2008). Dai et al. (2008)
reported that the spring maize yield increased by 1 600 kg
ha−1 on average, compared with those of summer maize in
the northwestern suburbs of Beijing. Consequently, adopting
spring maize to replace part of the winter wheat-summer
maize rotation system not only solves urgent agricultural
water-use problems in the NCP but also meets the demand
of food security (Dai et al. 2008; Liu et al. 2009; Tao et al.
2013b; Yuan et al. 2014). Therefore, the key to success
of this alternative model is to ensure that the spring maize
gain is high-yielding. Nevertheless, according to present
research and production conducted in southern Hebei
Province, the stably obtained yield in the spring maize
system only accounts for 56.9−66.3% of that in the winter
wheat-summer maize system (Tao 2013). One of the main
reasons for the limited spring maize high-yield is high-tem-
perature stress (HTS) at the grain-filling stage in the NCP,
especially in the southern part of NCP (Zheng et al. 2001;
Li et al. 2003; Tao et al. 2013b). To solve this problem,
previous research has explored methods of adjusting the
spring maize sowing dates and selecting varieties (Liu et al.
2009). However, the yield was still insufficient to consider
adopting spring maize to replace the winter wheat-summer
maize rotation system. Some reports have discussed
water and fertilization management to reduce HTS during
the summer maize grain-filling stage in the southern part of
NCP (Zhang 2003). However, corresponding technological
approaches to control HTS at the spring maize grain-filling
stage are limited, and research on the mechanism is insuf-
ficient. Therefore, the mechanism for why spring maize
suffers from HTS must be understood. Integrating individual
technologies to form a comprehensive technology system
may be a successful approach to achieve a high spring
maize yield in the NCP. This study summarizes the impact
of HTS on photosynthetic characteristics and water status
in maize to provide a clear direction for research in this field.
2. The high-temperature stress threshold
of the duration and rate in grain filling
HTS at the grain-filling stage of spring maize may reduce
the grain-filling rate and shorten the grain-filling stage to
lower the kernel weight (Tao et al. 2013b; Mayer et al.
2014). The grain linear growth period of silking to maturity
(25 d) decreased 7−15 d, and grain weight per plant (124 g)
decreased 16.9−44.4% when the maize was exposed to
day/night 30/15−35/25°C until 18 days post-silking (Jones
et al. 1981; Badu-Apraku et al. 1983). The grain-filling rate
decreases, kernel weight decreases by 7%, and the activ-
ity of adenosine diphosphate glucose pyrophosphorylase
declines from 15 d after pollination until maturity, under
a day/night temperature treatment of 33.5/25°C (Wilhelm
et al. 1999). The appropriate average daily temperature
for summer maize at the grain-filling stage (63−92 d after
emergence) is 24−26°C in Shandong Province, NCP, the
grain-filling rate decreases with increasing temperature
when the average daily temperature is 26−45°C (Li et al.
 TAO Zhi-qiang et al. Journal of Integrative Agriculture 2016, 15(12): 2677–2687
2003; Zhang 2003, 2005). Tao et al. (2013a) conducted a
path analysis on meteorological ecological factors (mean
daily temperature, days daily maximum temperatures
of ≥33°C, diurnal temperature, rainfall, sunshine hours),
1 000-kernel weight and kernel number for spring maize
at the grain-filling stage in the southern part of NCP. The
results showed that 6−17 d daily maximum temperatures
of ≥33°C had a negative effect on the kernel weight. In
conclusion, the HTS threshold for spring maize are a value
of daily mean temperature or day/night at which the grain
linear growth period is shortened and the grain-filling rate
is decreased, and that threshold vary in maize varieties
belonging to different habitats. However, the reports for the
HTS threshold in spring maize are insufficient in the NCP.
Thus, it is highly desirable to appraise the HTS threshold
for the grain linear growth period and the grain-filling rate in
spring maize to prevent damages by unfavorable tempera-
tures during grain filling in this region.
3. Physiological responses of maize
during grain filling to HTS
3.1. Photosynthesis
Photosynthesis is the most sensitive symptom to high tem-
perature compared with other stress symptoms and is easily
suppressed (Berry and Björkman 1980). Ben-Asher et al.
(2008) reported that the net photosynthetic rate (Pn) was
50−60% lower in maize under high temperature conditions
of 35/30°C (day/night) and 40/35°C (day/night) compared
to that under low-temperature conditions of 25/20°C (day/
night) and 30/25°C (day/night). The decreased Pn reduces
the supply of photosynthates to grain filling, and the lack
of photosynthates is one reason for the reduction of grain
yield and biomass (Reed and Singletary 1989; Edreira and
Otegui 2012), which occurs because plants under HTS
during the grain-filling period use further photosynthates to
cope with the stress (Badu-Apraku et al. 1983; Wahid et al.
2007). Thus, maize plants need good photosynthesis to
produce adequate photosynthates to carry out grain filling
under HTS. Here, we describe inhibited photosynthesis by
high temperatures in three areas.
High-temperature stress damages the thermal stability
of thylakoid membrane High temperature affects maize
growth throughout its life cycle, including all enzyme reac-
tions, metabolic functions and cell structural integrity, partic-
ularly membrane structure and properties, which have direct
bearing on survival. The membrane fatty acid composition
changes in response to heat stress, relative membrane per-
meability increases, and membrane structure and function
change, thus causing a series of physiological changes (Chen
and Burris 1991). This was related to activated oxygen spe-
2679
cies (AOS) including singlet oxygen (1O2), superoxide radical
(O2-.), hydrogen peroxide (H2O2) and hydroxyl radical (OH−)
accumulate to cause membrane lipid peroxidation and an
increased malondialdehyde (MDA) content and also prompt
Rubisco degradation in maize subjected to HTS (Gong et al.
1997; Hasanuzzaman et al. 2013).
Chloroplasts are the structural foundation of photosyn-
thesis and the basic photosynthetic organelle comprising
thylakoids and a matrix. The thylakoid membrane is the
photosynthetic photoreaction infrastructure (photosynthetic
electron transport and phosphorylation). The light-harvest-
ing pigment-protein complexes that absorb light energy,
such as photosystem I (PSI), photosystem II (PSII), the
cytochrome b6f complex (Cyt b6f), ATP synthase, and related
electron transfer factors, are all located in the thylakoid mem-
brane. Therefore, under stress conditions, maintaining the
stability of the thylakoid membrane is particularly important
for photosynthesis (Blum 1988). The thylakoid membrane
structure is very sensitive to high temperature, and heat
stress decreases its integrity and increases membrane
permeability (Yang et al. 1996; Savchenko et al. 2002) to
release electrolytes from the cell and reduce thermal stability
of the cell membrane (Wahid et al. 2007). This could be
not conducive to photosynthesis. However, superoxide dis-
mutase (SOD), catalase (CAT), peroxidase (POD), ascorbic
acid enzyme (APX), and glutathione reductase (GR) could
scavenge AOS produced by HTS and protect thermal sta-
bility of the cell membrane (Matters and Scandalios 1986;
Obata et al. 2015).
High-temperature stress reduces chlorophyll and dis-
rupts electron transfer to limits photosynthesis Most
chlorophyll acts as antennae in the pigment bed. And the
electron transport chain is the key link in photosynthesis that
forms assimilatory power. However, HTS reduces chloro-
phyll and disrupts electron transfer to limits photosynthesis.
Karim et al. (1999) and Zhu et al. (2011) reported that heat
stress reduces chlorophyll a and chlorophyll b contents,
leading to Pn is limited in maize plants.
Depressed electron transfer functioning is one reason
for the rapid decrease in maize leaf photosynthetic capacity
under stress (Zong et al. 2014). PSI and PSII comprise a
two-reaction system in the electron transfer. The PSI and
PSII electron transfer processes are similar, as the two opti-
cal systems are in an electron transfer series; thus, reduced
efficiency in one will cause lower photosynthetic efficiency as
a whole (Redding et al. 1999). Zhang et al. (2013) reported
that the quicker decrease in PSI and PSII photochemistry
activities and severer deterioration of electron transfer
activity are two of the most important reasons to decrease
photosynthetic capacity in maize leaves. In addition, PSII
is sensitive to heat, PSII has protein complexes located
in the thylakoid membrane, and HTS destroys membrane
2680 TAO Zhi-qiang et al. Journal of Integrative Agriculture 2016, 15(12): 2677–2687
stability and proteins, which lowers or terminates its activity
(Mcdonald and Paulsen 1997; Bukhov et al. 1999), resulting
in decreasing the actual quantum yields of PSII electron
transfer (ФPSII) and the photosynthetic rate (Yang et al. 1996;
Sinsawat et al. 2004).
High-temperature stress decreases photosynthetic
carbon assimilation HTS decreases photosynthetic
carbon assimilation, as it decreases pyruvate carboxylase
enol phosphate (PEPC) and Rubisco activity, which does
not favor the carboxylation reaction or the Calvin cycle.
e.g., Rubisco activity decreases when temperatures are
>32.5°C, and no activity occurs when the temperature
is 45°C (Crafts-Brander and Salvucci 2002). PEPC and
Rubisco activities in summer maize (Nongda 108) ear
blades decreased by 51.1 and 51.1%, respectively, when
the plants were grown at daily mean temperature 28.4°C
(3.1°C higher than the control) from flowering to maturity
in Shandong Province, NCP (Zhang 2005). The heat-tol-
erant maize genotype Xundan 20 has more PEPCase and
RuBPCase activities of ear-leaves than the heat-sensitive
maize genotype Zhuyu 309 when the maize was exposed
to 8 d daily mean temperatures of ≥35°C 0−8 d post-silking
in Henan Province, NCP (Zhao et al. 2012).
3.2. Water relations
Water deficit will occur on maize plants when water con-
sumption is greater than absorption at the grain-filling stage
under HTS. Firstly, atmospheric high temperature causes
a water deficit. Stomata are forced to close when the plant
water loss is greater than the root water-absorbing capacity,
leading to decreased photosynthetic activity when the air
temperature is high and the relative humidity is low, which
occurs due to the high transpiration rate even if sufficient soil
water exists (Muchow and Sinclair 1991; Karim et al. 2001).
Secondly, a water deficit is caused by high soil temperatures,
whereby higher soil temperatures lead to faster soil surface
moisture evaporation rates, which inhibits downward ex-
tension of roots and decreases root hydraulic conductivity,
leading to water deficit (Veen 1982; Ding et al. 2007).
Water deficit has important effects on grain filling at the
grain-filling stage in maize under HTS. Borrás and Westgate
(2006) reported that maize kernel weight is closely related
to the water supply during rapid grain filling. High tempera-
ture (35°C) decreases the water potential, which inhibits
grain-filling rate, leading to falling of kernel weight by 45%
in maize (Singletary et al. 1994). Turgor pressure (or water
potential) shapes leaf and root morphology and controls
guard cells for gas exchange to produce photosynthates.
When water deficit happens, the turgor pressure (or water
potential) decreases, leading to stomatal closure (Schoper
et al. 1986; Ristic et al. 1992; Hirasawa et al. 1999), and leaf
curl (Michelena and Boyer 1982; Cramer 1992), inhibited
root growth (Veen 1982), and decreased leaf relative water
content by 10−20%, limited stomatal conductance (gs) and
Pn at 35 and 40°C treatments for 1 wk in maize (Zhu et al.
2011), resulting in bad photosynthesis to produce insufficient
photosynthates to carry out grain filling under HTS. Boyle
et al. (1991) reported that decreased water potential inhib-
its photosynthetic capacity at the maize grain-filling stage,
limits the transport of leaf photosynthates to the grain, and
shortens the grain-filling stage, decreasing grain weight.
3.3. Hormonal (abscisic acid) changes
Plants must have effective communication among cells,
tissues and organs to coordinate growth and development
and adapt to the environment. The shoot and root of plants
are in different environments and rely on the vascular bundle
as a contact point. Abscisic acid (ABA), a chemical mes-
senger, a plant secondary metabolite and a hormone, has
an important role regulating plant growth and development.
ABA is generated from the maize root and is transported
in the xylem and phloem through the vascular bundle to
indirectly affect the root and branch hydraulic conductivity,
as well as the amount, diameter, dry weight (Rivier et al.
1977; Reed and Singletary 1989; Giuliani et al. 2005), leaf
senescence (Zhang and Davies 1990), gs and transpiration
(Rodriguez and Davies 1982; Ribaut and Pilet 1991; Tardieu
et al. 1992; Jovanović et al. 2000), and Pn in maize (Schraut
et al. 2004; Zhu et al. 2011), affecting photosynthates to
carry out grain filling under HTS. Cheikh and Jones (1994)
exposed maize to heat stress (35°C) for 4 and 8 d at 3 days
post-pollination (25°C), and found decreased kernel weight
and decreased yield, caused by a significantly increased
ABA concentration in the ear.
4. Mechanism of heat tolerance are formed
through signal transduction
The process of information transmission occurs at the
cellular level and the overall level of the plant when maize
suffers HTS. At the cellular level, ABA activates HSPs genes
in response to HTS. HSPs act as molecular chaperones,
participate in protein refolding and degradation caused by
HTS, and stabilize the target protein configuration to en-
hance heat tolerance in maize (Kotak et al. 2007). When the
extracellular signal (e.g., ABA) transfers heat information to
a living cell, the cells transport information to the intracellular
membrane receptor (Ballio et al. 1981; McCarty et al. 1989)
and downstream membrane proteins in maize (Zhang et al.
2006). Then, Ca2+ acts as an intracellular second messen-
ger (Hu et al. 2007) to pass the signal further and affect gene
expression and regulation in maize (Heikkila et al. 1984;
 TAO Zhi-qiang et al. Journal of Integrative Agriculture 2016, 15(12): 2677–2687
Gullìa et al. 2005). HSPs act as molecular chaperones
(Sun et al. 2000) to protect other proteins and improve the
activities of antioxidant enzymes (e.g., SOD, CAT, APX, and
GR) and to alleviate membrane damage caused by reactive
oxygen species (ROS) in maize (Jiang and Zhang 2002; Hu
et al. 2010). HSPs can also combine with modified proteins
to maintain a soluble state (Gagliardi et al. 1995; Young et al.
2001; Marrs et al. 2005), which are conductive to maintain
the thermal stability of thylakoid membrane, chlorophyll,
electron transfer, PEPC, and Rubisco activity to improve
photosynthesis. And ABA induces stomatal closure to
maintain a good plant water status (Jovanović et al. 2000).
Ultimately, improved photosynthesis and maintained plant
water status enhance heat tolerance under HTS.
5. Strategies specified for thermotoler-
ance acquired in spring maize for the NCP
Based on above elaboration, several methods were dis-
cussed as strategies to avoid and tolerate HTS at the
grain-filling stage of maize in NCP. These ideas include
adjusting sowing date to avoid HTS, breeding heat-tolerance
varieties, and tillage methods, optimizing irrigation, heat
acclimation, regulating chemicals, nutritional management,
and planting geometric design to tolerate HTS.
5.1. Avoid high-temperature stress by sowing date
adjusting
Advancing or delaying sowing date is strategy to avoid HTS.
Liu et al. (2013) reported that earlier sowing dates and lon-
ger season varieties have overcome the negative effects of
climate warming on spring maize yield in Northeast China.
Dai et al. (2009) results showed that sowing date from late
April to late May, mean daily temperature decreased 1.7 and
4.3°C, diurnal temperature range increased 4.3 and 3.1°C
during grain filling middle stage (16 to 45 d after silking)
and grain filling late stage (45 d after silking to maturity),
respectively. The decrease of mean daily temperature and
the increase of diurnal temperature range led to extend
spring maize green leaves duration, increased 1 000-kernel
weight by 4.3%, grain yield by 17.6%, respectively, in spring
maize in Beijing City, NCP. Tao (2013) and Tao et al. (2013a)
reported that HTS (daily maximum temperature of ≥33°C
and mean daily temperature >26°C) happens from June to
August, grain filling stage in spring maize meets HTS from
sowing date early April to late May, resulting in the direct
negative effects on 1 000-grain weight. But 1 000-grain
weight of spring maize sown in mid May was higher than that
of other sowing date treatments, because of avoiding high
temperature stress during the grain-filling period (compared
with other sowing dates, the treatment with sowing dates of
2681
mid May had decreased ≥33°C d of 2−7 d and mean daily
temperature 0.5−1.3°C), plants maintained stability of cell
membrane, chlorophyll content, and plant water status,
which are beneficial to photosynthesis, and prolonged
quickly increase period 0.2−0.6 d, increased mean rate of
grain filling 0.10−0.66 mg grain−1 d−1, produced higher grain
weight in Wuqiao County, Hebei Province in NCP.
5.2. Tolerate high-temperature stress from seven
strategies
Variety As different varieties respond differently to HTS,
breeding heat-tolerance varieties is an effective strategy to
improve heat tolerance at the spring maize grain-filling stage;
e.g., Nongda 108 compared to Ludan 50, Shannong 3,
Liaoyu 5, Yedan 2, and Luyuandan 14, grain yield was the
highest under high temperature in Shandong Province,
NCP (Zhang 2003). Selection criteria have been proposed
in traditional breeding to facilitate detection of heat-tolerant
spring maize variety; e.g., Tianyu 198 compared to Xingyu
998 and Tianrun 606, stress tolerance indices, chlorophyll
content, leaf area index, and photosynthetically active radia-
tion were highest under high temperature in Hebei Province,
NCP (Tao et al. 2016). In addition, traditional protocols,
marker-assisted selection (MAS) and genetic transgenic
approaches have contributed significantly to a better improv-
ing of heat tolerance in maize (Gu et al. 2015; Obata et al.
2015). Heat shock protein 70 (HSP70) enhances the anti-
oxidant capacity and photosynthetic characteristics in maize
leaves under HTS: e.g., compared with Zhengdan 958,
Xundan 20 and Zhuyu 309, Longyu 602 showed a higher
heat tolerance, because of its leaves had less MDA, and
more APX, GR, SOD, and CAT in Henan Province, NCP
(Hu et al. 2010; Zhao et al. 2012). Tao (2013) reported that
SOD increased and MDA decreased in maize ear leaf for
enhancing the stability of cell membrane, which helps to
improve photosynthesis for good grain filling characteristics
(long quickly increase period and high mean rate of grain
filling), so that high kernel weight was produced under HTS
in Wuqiao County, Hebei Province in NCP. According to
these results, we can achieve heat-tolerance varieties at
the grain-filling stage in spring maize through a combination
of traditional breeding methods and modern biotechnology.
Tillage method An appropriate tillage method improves soil
water conditions to promote maize growth and development
under HTS, e.g., compared to plowing, subsoiling (or deep
ploughing) with straw mulching increases kernel weight
and yield of spring maize by directly improving soil moisture
and root growth and indirectly improving the plant water
status, increasing the chlorophyll content, Pn and gs, and
grain-filling rate in Shandong and Henan provinces, NCP
(Hu et al. 2011; Zhao et al. 2014), extending the grain-filling
2682 TAO Zhi-qiang et al. Journal of Integrative Agriculture 2016, 15(12): 2677–2687
stage to higher the kernel weight in Hebei Province, NCP
(Tao et al. 2013b). These studies can provide a theoretical
basis for improving yield of maize under HTS by adjusting
soil tillage in the NCP.
Optimizing irrigation In the vegetative growth period under
soil drought stress and atmospheric high temperature could
delay the process of growth of spring maize and shorten
the reproductive stage, but those were improved in the
condition of that the soil moisture content was maintained
65% field capacity by drip irrigation in Hebei Province,
NCP (Yuan et al. 2014). Increasing the irrigation time and
an unchanged irrigation volume improves heat tolerance
and increases kernel weight, and yield in summer maize in
Shandong Province, NCP (Zhang 2003). Optimizing soil
water improves leaf moisture status of maize seedlings
under high temperatures (35 and 40°C) and enhances the
heat tolerance of maize (Zhu et al. 2011). Thus, optimizing
irrigation has the potential to improve the water status of
maize to enhance its heat tolerance.
Heat acclimation Heat acclimation refers to developing
increased heat tolerance in maize after gradually increasing
the temperature to the HTS threshold (Gong et al. 2001;
Crafts-Brander and Salvucci 2002). Sinsawat et al. (2004)
reported that exposing maize to >45°C causes permanent
damages to its photosynthetic ability; maize seedlings
placed the first in a 41°C environment and then at 50°C
did not have different photosynthetic rates, indicating that
maize seedlings developed heat tolerance by acclimating
to the 41°C environment. Thus, heat acclimation is a strat-
egy to improve heat tolerance at the grain-filling stage in
spring maize.
Chemical regulation Plant hormones and exogenous
chemicals (e.g., ABA and CaCl2) play important roles in
strengthening heat tolerance in maize under HTS. Exoge-
nous ABA induces maize to produce HSPs, strengthening
PSII heat tolerance (Gong et al. 1998; Maestri et al. 2002).
An exogenous CaCl2 increases the maize cell membrane
antioxidant capacity to improve heat tolerance (Gong et al.
1997).
Nutrient management Maize physiological function
decreases under abiotic stress but can be compensated
for by nutritional management, e.g., adequate potassium
fertilizer improves cell membrane stability, turgor pressure,
water potential in maize under water-deficit conditions
(Premachandra et al. 1991). The nitrogen content in
maize leaves improves the photosynthetic radiation-use
efficiency and CO2 assimilation rate (Muchow and Sinclair
1994). Plastocyanin is a copper-containing component of
the photosynthetic electron transport chain and an electron
carrier between Cyt b6f and PSI. Thus, a lack of copper is
not conducive to maize photosynthetic electron transport
(Ouzounidou et al. 1997). A lack of phosphorus in maize
reduces the leaf photosynthetic active radiation interception
rate, reduces the carbon supply from leaves to roots, and
inhibits root growth (Mollier and Pellerin 1999). Zinc defi-
ciency in maize decreases Pn, gs, Fv/Fm, and SOD activity
but increases the MDA content (Wang and Jin 2005). In
short, a lack of nutrient elements was not conducive to
cell membrane stability, turgor pressure, water potential,
photosynthetic electron transport, root growth, and Pn in
maize plant, these symptoms were similar to those of HTS
in maize plant. Thus, a strategy to improve heat tolerance in
spring maize at the grain-filling stage is to regulate nutrition.
Planting geometric design It is conducive to improving
temperature and relative humidity of field and the use
efficiency of light and heat to change the planting spatial
layout of maize by deploying plant distance and row width, as
well as it is one of the feasible methods to improve the yield
of maize in Shandong and Hebei provinces, NCP (Li et al.
2012; Wu et al. 2012). The latest research indicated that the
spring maize population structure and shoot morphological
structure under high-density condition were effectively reg-
ulated by the clumped and scattered planting geometries,
which improved photosynthesis capacity of middle-down
leaves at the filling stage and revealed a great potential of
high-yielding structure and tolerance to high-density planting
in Hebei Province, NCP (Wu et al. 2015). Thus, planting
geometric design is a strategy conducive to improving the
micro-environment (temperature and humidity) in spring
maize group under HTS for improving photosynthesis to
enhance heat tolerance during the grain-filling period in
Hebei Province, NCP.
6. Conclusion
Spring maize suffers HTS, which restricts production during
the grain-filling period in the NCP. The cause is that the HTS
destroys the chloroplast, limits the absorption and trans-
mission of light energy, disturbs electron transfer, reduces
photosynthetic carbon assimilation, inhibits photosynthesis,
and decreases the plant water potential and turgor pressure
to induce a water deficit in spring maize at the grain-filling
stage. Restricted photosynthesis and water status lead to
insufficient photosynthates to the grain filling, resulting in
lower kernel weight and yield. However, the maize plant
transduces ABA signal to express HSPs, which are molec-
ular chaperones that participate in protein refolding and
degradation caused by HTS. HSPs stabilize target protein
configurations and indirectly improve thylakoid membrane
structure stability, light energy absorption and passing,
electron transport, and fixed carbon assimilation, leading
to improved photosynthesis. ABA induces stomatal closure
to maintain a good plant water status. Ultimately, improved
photosynthesis and maintained plant water status enhance
 TAO Zhi-qiang et al. Journal of Integrative Agriculture 2016, 15(12): 2677–2687 2683

heat tolerance during the grain-filling period, resulting in
higher kernel weight and yield (Fig. 1).
We have discussed how to increase spring maize heat
tolerance using cultivation and tillage techniques under HTS
at the grain-filling stage. Tolerance and avoidance describe
our plan to solve the problem, e.g., to improve the plant
water status and photosynthesis, promote the production of
assimilates and the transport and distribution to the grain,
improve the grain-filling rate, extend the grain-filling period,
increase the kernel weight, and increase the yield. Specific
technologies include choosing a sowing date that avoids
HTS at the grain-filling stage and breeding tolerant varieties,
and exploring reasonable control technology (e.g., tillage
method, irrigation, heat acclimation, chemicals regulation,

High temperature stress

HSPs HSP chaperone Root growth ↓

Antioxidant enzyme
Water potential ↓
ABA in xylem
Reactive oxygen ↑ Transpiration ↑
Pigment protein Protein complex PEPC and Rubisco
denaturation activity of PSII ↓ activities ↓
Membrane lipid peroxidation Water consumption
Chl content ↓
↑ more than absorption

Thylakoid membrane Light energy absorption Electron transport ↓ Fixed carbon Leaf water potential↓
structure stability ↓ and passing ↓ assimilation ↓ Turgor ↓
membrane permeability ↑ Leaf RWC ↓

Stomatal conductance ↓
Photosynthesis ↓
Maintenance of plant water

Grain yield ↓ Kernel weight ↓ Filling rate and duration ↓ The supply of photosynthates to the grain ↓

Fig. 1 High temperature stress mechanism in maize black arrows, and denote the process of high temperature stress, the increase
and decrease of reaction substance or physiological state, respectively; blue arrows, and denote increased heat tolerance by ABA
signal transduction process, the increase and decrease of reaction substance or physiological state, respectively. Chl, chlorophyll;
HSPs, heat shock proteins; ABA, abscisic acid; PEPC, pyruvate carboxylase enol phosphate; RWC, relative water content.

Strategies specified Physiological basis of alleviating high-temperature stress during grain filling

Avoid HTS Sowing date

Thylakoid membrane
Variety
structure stability
Grain filling rate
Heat acclimation Photosynthesis
Chlorophyll and duration

Chemical regulation Gas exchange

Tolerate HTS Nutrient management

Leaf relative
Planting geometric water content
design

Tillage method Soil water

and root
Optimizing irrigation

Fig. 2 Strategies specified for alleviating high-temperature stress and physiological basis during grain filling in spring maize for
the NCP.
2684 TAO Zhi-qiang et al. Journal of Integrative Agriculture 2016, 15(12): 2677–2687
nutrient management and planting geometric design) to
improve heat tolerance (Fig. 2).
The focus of further studies should be to conduct a
spring maize sowing date field experiment and analyze
meteorological factors, so one sowing date can be identified
that avoids heat stress at the grain-filling stage; develop a
thorough understanding of the causes and impacts (i.e.,
morphology, physiology, molecules, hormones, and second-
ary metabolites) of heat stress on spring maize during the
entire growth period; establish an evaluation index system
under heat stress at the grain-filling stage; explore a rapid,
simple, and scientific heat-tolerance evaluation method in
spring maize and provide a theoretical basis for heat-toler-
ance breeding in spring maize; and develop effective single
cultivation and tillage technology to avoid and tolerate HTS
and increase heat tolerance based on a systematic design
to form a comprehensive technical system.
Acknowledgements
This work was supported by the National Natural Science
Fundation of China (31571601) and the Special Scientific
Research Fund of Agricultural Public Welfare Profession of
China (201503121-11).
References
Badu-Apraku B, Hunter R B, Tollenaar M. 1983. Effect of
temperature during grain filling on whole plant and grain
yield in maize (Zea mays L.). Canadian Journal of Plant
Science, 63, 357−363.
Ballio A, Federico R, Scalorbi D. 1981. Fusicoccin structure-
activity relationships: In vitro binding to microsomal
preparations of maize coleoptiles. Physiologia Plantarum,
52, 476−481.
Ben-Asher J, Garcia A G Y, Hoogenboom G. 2008. Effect of
high temperature on photosynthesis and transpiration of
sweet corn (Zea mays L. var. rugosa). Photosynthetica,
46, 595−603.
Berry J, Björkman O. 1980. Photosynthetic response and
adaptation to temperature in higher plants. Annual Review
of Plant Physiology, 31, 491−543.
Blum A. 1988. Plant Breeding for Stress Environments. CRC
Press, Boca Raton, Florida. p. 223.
Borrás L, Westgate M E. 2006. Predicting maize kernel sink
capacity early in development. Field Crops Research, 95,
223−233.
Boyle M G, Boyer J S, Morgan P W. 1991. Stem infusion of
liquid culture medium prevents reproductive failure of maize
at low water potential. Crop Science, 31, 1246−1252.
Bukhov N G, Wiese C, Neimanis S, Heber U. 1999. Heat
sensitivity of chloroplasts and leaves: Leakage of protons
from thylakoids and reversible activation of cyclic electron
transport. Photosynthesis Research, 59, 81−93.
Cheikh N, Jones R J. 1994. Disruption of maize kernel growth
and development by heat stress. Plant Physiology, 106,
45−51.
Chen Y, Burris J S. 1991. Desiccation tolerance in maturing
maize seed: Membrane phospholipid composition and
thermal properties. Crop Science, 31, 766−770.
Crafts-Brander C, Salvucci M. 2002. Sensitivity to photosynthesis
in the C4 plant, maize to heat stress. The Plant Cell, 12,
54−68.
Cramer G R. 1992. Kinetics of maize leaf elongation II.
responses of a Na-excluding cultivar and a Na-including
cultivar to varying Na/Ca salinities. Journal of Experimental
Botany, 43, 857−864.
Dai M H, Tao H B, Binder J, Wang L N, Claupein W, Wang P.
2008. Comparing grain production and utilization of solar,
heat resources between spring maize and summer maize.
Journal of Maize Sciences, 16, 82−85, 90. (in Chinese)
Dai M H, Shan C G, Wang P. 2009. Effect of temperature and
solar ecological factors on spring maize production. Journal
of China Agricultural University, 14, 35−41. (in Chinese)
Ding W, Cai Y, Cai Z, Yagi K, Zheng X. 2007. Soil respiration
under maize crops: Effects of water, temperature, and
nitrogen fertilization. Soil Science Society of America
Journal, 71, 944−951.
Edreira J I R, Otegui M E. 2012. Heat stress in temperate and
tropical maize hybrids: Differences in crop growth, biomass
partitioning and reserves use. Field Crops Research, 123,
62−73.
Gagliardi D, Breton C, Chaboud A, Vergne P, Dumas C. 1995.
Expression of heat shock factor and heat shock protein 70
genes during maize pollen development. Plant Molecular
Biology, 29, 841−856.
Giuliani S, Sanguineti M C, Tuberosa R, Bellotti M, Salvi S,
Landi P. 2005. Root-ABA1, a major constitutive QTL,
affects maize root architecture and leaf ABA concentration
at different water regimes. Journal of Experimental Botany,
56, 3061−3070.
Gong M, Chen B, Li Z G, Guo L H. 2001. Heat-shock-induced
cross adaptation to heat, chilling, drought and salt stress in
maize seedlings and involvement of H2O2. Journal of Plant
Physiology, 158, 1125−1130.
Gong M, Chen S N, Song Y Q, Li Z G. 1997. Effect of calcium
and calmodulin on intrinsic heat tolerance in relation to
antioxidant systems in maize seedlings. Australian Journal
of Plant Physiology, 24, 371−379.
Gong M, Li Y J, Chen S Z. 1998. Abscisic acid-induced
thermotolerance in maize seedlings is mediated by calcium
and associated with antioxidant systems. Journal of Plant
Physiology, 153, 488−496.
Gu L, Zhang Y M, Zhang M S, Li T, Dirk L M A, Downie B,
Zhao T Y. 2015. ZmGOLS2, a target of transcription factor
ZmDREB2A, offers similar protection against abiotic stress
as ZmDREB2A. Plant Molecular Biology, 90, 157−170.
Gullìa M, Rampinob P, Lupottoc E, Marmirolia N, Perrotta C.
2005. The effect of heat stress and cadmium ions on the
expression of a small hsp gene in barley and maize. Journal
 TAO Zhi-qiang et al. Journal of Integrative Agriculture 2016, 15(12): 2677–2687
of Cereal Science, 42, 25−31.
Hasanuzzaman M, Nahar K, Alam M M, Roychowdhury R,
Fujita M. 2013. Physiological, biochemical, and molecular
mechanisms of heat stress tolerance in plants. International
Journal of Molecular Sciences, 14, 9643–9684.
Heikkila J J, Papp J E T, Schultz G A, Bewley J D. 1984.
Induction of heat shock protein messenger RNA in maize
mesocotyls by water stress, abscisic acid, and wounding.
Plant Physiology, 76, 270−274.
Hirasawa T, Hsiao T C. 1999. Some characteristics of reduced
leaf photosynthesis at midday in maize growing in the field.
Field Crops Research, 62, 53−62.
Hu H Y, Li Z J, Ning T Y, Wang Y, Tian S Z, Zhong W L, Zhang
Z Z. 2011. Effects of subsoiling and urea types on water use
efficiency of different maize cultivars. Scientia Agricultura
Sinica, 44, 1963−1972. (in Chinese)
Hu X L, Jiang M Y, Zhang J H, Zhang A Y, Lin F, Tan M P.
2007. Calcium-calmodulin is required for abscisic acid-
induced antioxidant defense and functions both upstream
and downstream of H2O2 production in leaves of maize (Zea
mays) plants. New Phytologist, 173, 27−38.
Hu X L, Li C H, Yang H R, Liu Q J, Li C H. 2010. Heat shock
protein 70 may improve the ability of antioxidant defense
induced by the combination of drought and heat in maize
leaves HSP70. Acta Agronomica Sinica, 36, 636−644. (in
Chinese)
Jiang M Y, Zhang J H. 2002. Water stress-induced abscisic acid
accumulation triggers the increased generation of reactive
oxygen species and up-regulates the activities of antioxidant
enzymes in maize leaves. Journal of Experimental Botany,
53, 2401−2410.
Jones R J, Gengenbach B G, Cardwell V B. 1981. Temperature
effects on in vitro kernel development of maize. Crop
Science, 21, 761−766.
Jovanović L, Stikić R, Hartung W. 2000. Effect of osmotic stress
on abscisic acid efflux and compartmentation in the roots of
two maize lines differing in drought susceptibility. Biologia
Plantarum, 43, 407−411.
Karim M A, Fracheboud Y, Stamp P. 1999. Photosynthetic
activity of developing leaves of Zea mays is less affected
by heat stress than that of developed leaves. Physiologia
Plantarum, 105, 685−693.
Karim M A, Fracheboud Y, Stamp P. 2001. Effect of high
temperature on seedling growth and photosynthesis of
tropical maize genotypes. Journal of Agronomy and Crop
Science, 184, 217−223.
Kotak S, Larkindale J, Lee U, Koskull-Döring P V, Vierling E,
Scharf K D. 2007. Complexity of the heat stress response
in plants. Current Opinion in Plant Biology, 10, 310−316.
Leitner D, Meunier F, Bodner G, Javaux M, Schnepf A. 2014.
Impact of contrasted maize root traits at flowering on
water stress tolerance - A simulation study. Field Crops
Research, 165, 125−137.
Li J M, Inanaga S, Li Z H, Eneji A E. 2005. Optimizing irrigation
scheduling for winter wheat in the North China Plain.
Agricultural Water Management, 76, 8−23.
2685
Li S C, Bai P, Lu X, Liu S Y, Dong S T. 2003. Ecological and
sowing date effects on maize grain filling. Acta Agronomica
Sinica, 29, 775−778. (in Chinese)
Liu M, Tao H B, Wang P, Zhang Y J. 2009. Effects of sowing
date on growth, yield formation and water utilization of
spring maize. Journal of Maize Sciences, 17, 108−111.
(in Chinese)
Liu Z J, Hubbard K G, Lin X M, Yang X G. 2013. Negative
effects of climate warming on maize yield arereversed by the
changing of sowing date and cultivarselection in Northeast
China. Global Change Biology, 19, 3481−3492.
Li Z X, Chen Y Q, Wang Q C, Liu K C, Zhang X Q, Liu X, Zhang
H, Liu S C, Liu C X, Gao W S, Sui P. 2012. Effect of different
planting methods on root-shoot characteristics and grain
yield of summer maize under high densities. Acta Ecologica
Sinica, 32, 7391−7401. (in Chinese)
Maestri E, Klueva N, Perrotta C, Gulli M, Nguyen, H T, Marmiroli
N. 2002. Molecular genetics of heat tolerance and heat
shock proteins in cereals. Plant Molecular Biology, 48,
667−681.
Marrs K A, Casey E S, Capitant S A, Bouchard R A, Dietrich
P S, Mettler I J, Sinibaldi R M. 2005. Characterization of
two maize HSP90 heat shock protein genes: Expression
during heat shock, embryogenesis, and pollen development.
Developmental Genetics, 14, 27−41.
Ma S Y, Yu Z W, Shi Y, Gao Z Q, Luo L P, Chu P F, Guo Z J.
2015. Soil water use, grain yield and water use efficiency
of winter wheat in a long-term study of tillage practices
and supplemental irrigation on the North China Plain.
Agricultural Water Management, 150, 9−17.
Matters G L, Scandalios J G. 1986. Effect of elevated
temperature on catalase and superoxide dismutase during
maize development. Differentiation, 30, 190−196.
Mayer L I, Edreira J I R, Maddonni G A. 2014. Oil yield
components of maize crops exposed to heat stress during
early and late grain-filling stages. Crop Science, 54,
2236−2250.
McCarty D R, Carson C B, Stinard P S, Robertson D S. 1989.
Molecular analysis of viviparous-1: An abscisic acid-
insensitive mutant of maize. The Plant Cell, 1, 523−532.
Mcdonald G K, Paulsen G M. 1997. High temperature effects
on photosynthesis and water relations of grain legumes.
Plant Soil, 196, 47−58.
Michelena V A, Boyer J S. 1982. Complete turgor maintenance
at low water potentials in the elongating region of maize
leaves. Plant Physiology, 69, 1145−1149.
Mollier A, Pellerin S. 1999. Maize root system growth and
development as influenced by phosphorus deficiency.
Journal of Experimental Botany, 50, 487−497.
Muchow R C, Sinclair T R. 1991. Water deficit effects on maize
yields modeled under current and “greenhouse” climates.
Agronomy Journal, 83, 1052−1059.
Muchow R C, Sinclair T R. 1994. Nitrogen response of leaf
photosynthesis and canopy radiation use efficiency in field-
grown maize and sorghum. Crop Science, 34, 721−727.
National Bureau of Statistics of the People’s Republic of
2686 TAO Zhi-qiang et al. Journal of Integrative Agriculture 2016, 15(12): 2677–2687
China. 2014. Regional data: annual data in various
provinces. [2016-01-01]. http://data.stats.gov.cn/easyquery.
htm?cn=E0103
Obata T, Witt S, Lisec J, Palacios-Rojas N, Florez-Sarasa I,
Yousfi S, Araus J L, Cairns J E, Fernie A R. 2015. Metabolite
profiles of maize leaves in drought, heat, and combined
stress field trials reveal the relationship between metabolism
and grain yield. Plant Physiology, 169, 2665−2683.
Ouzounidou G, Moustakas M, Strasser R J. 1997. Sites of
action of copper in the photosynthetic apparatus of maize
leaves: kinetic analysis of chlorophyll fluorescence, oxygen
evolution, absorption changes and thermal dissipation as
monitored by photoacoustic signals. Australian Journal of
Plant Physiology, 24, 81−90.
Premachandra G S, Saneoka H, Ogata S. 1991. Cell membrane
stability and leaf water relations as affected by potassium
nutrition of water-stressed maize. Journal of Experimental
Botany, 42, 739−745.
Redding K. Cournac L, Vassiliev I R, Golbeck J H, Peltier
G, Rochaix J D. 1999. Photosystem I is indispensable
for photoautotrophic growth, CO 2 fixation, and H 2
photoproduction. The Journal of Biological Chemistry, 274,
10466−10473.
Reed A J, Singletary G W. 1989. Roles of carbohydrate
supply and phytohormones in maize kernel abortion. Plant
Physiology, 91, 986−992.
Ribaut J M, Pilet P E. 1991. Effects of water stress on growth,
osmotic potential and abscisic acid content of maize roots.
Physiologia Plantarum, 81, 156−162.
Ristic Z, Gifford D J, Cass D D. 1992. Dehydration, damage
to the plasma membrane and thylakoids, and heat-shock
proteins in lines of maize differing in endogenous levels
of abscisic acid and drought resistance. Journal of Plant
Physiology, 139, 467−473.
Rivier L, Milon H, Pilet P E. 1977. Gas chromatography-mass
spectrometric determinations of abscisic acid levels in the
cap and the apex of maize roots. Planta, 134, 23−27.
Rodrigue Z J L, Davies W J. 1982. The effects of temperature
and ABA on stomata of Zea mays L. Journal of Experimental
Botany, 33, 977−987.
Savchenko G E, Klyuchareva E A, Abrabchik L M, Serdyuchenko
E V. 2002. Effect of periodic heat shock on the membrane
system of etioplasts. Russian Journal of Plant Physiology,
49, 349−359.
Schoper J B, Lambert R J, Vasilas B L. 1986. Maize pollen
viability and ear receptivity under water and high
temperature stress. Crop Science, 26, 1029−1033.
Schraut D, Ullrich C I, Hartung W. 2004. Lateral ABA
transport in maize roots (Zea mays): Visualization by
immunolocalization. Journal of Experimental Botany, 55,
1635−1641.
Singletary G W, Banisadr R, Keeling P L. 1994. Heat stress
during grain filling in maize: Effects on carbohydrate storage
and metabolism. Australian Journal of Plant Physiology,
21, 829−841.
Sinsawat V, LeiPner J, Stamp P, Fracheboud Y. 2004. Effect
of heat stress on the photosynthetic apparatus in maize
(Zea mays L.) grown at control or high temperature.
Environmental and Experimental Botany, 52, 123−129.
Sun X T, Li B, Zhou G M, Tang W Q, Bai J, Sun D Y, Zhou R G.
2000. Binding of the maize cytosolic Hsp70 to calmodulin,
and identification of calmodulin-binding site in Hsp70. Plant
and Cell Physiology, 41, 804−810.
Tao Z Q. 2013. Technologic solutions of high temperature
stress in spring maize during the filling stage in the North
China Plain. Ph D thesis, China Agricultural University,
China. (in Chinese)
Tao Z Q, Chen Y Q, Li C, Yuan S F, Shi J T, Gao W S, Sui P.
2013a. Path analysis between yield of spring maize and
meteorological factors at different sowing times in North
China Low Plain. Acta Agronomica Sinica, 39, 1628−1634.
(in Chinese)
Tao Z Q, Chen Y Q, Zou J X, Li C, Yuan S F, Yan P, Shi J T, Sui
P. 2016. Spectral characteristics of different heat tolerance
in spring maize varieties to high temperature. Spectroscopy
and Spectral Analysis, 36, 520−526. (in Chinese)
Tao Z Q, Sui P, Chen Y Q, Li C, Nie Z J, Yuan S F, Shi J T,
Gao W S. 2013b. Subsoiling and ridge tillage alleviate the
high temperature stress in spring maize in the North China
Plain. Journal of Integrative Agriculture, 12, 2179−2188.
Tardieu F, Zhang J, Katerji N, Bethenod O, Palmer S, Davies
W J. 1992. Xylem ABA controls the stomatal conductance
of field-grown maize subjected to soil compaction or soil
drying. Plant, Celt and Environment, 15, 193−197.
Veen B W. 1982. The influence of mechanical impedance on
the growth of maize roots. Plant and Soil, 66, 101−109.
Wahid A, Gelani S, Ashraf M, Foolad M R. 2007. Heat tolerance
in plants: An overview. Environmental and Experimental
Botany, 61, 199−223.
Wang H, Jin J Y. 2005. Photosynthetic rate, chlorophyll
fluorescence parameters, and lipid peroxidation of maize
leaves as affected by zinc deficiency. Photosynthetica, 43,
591−596.
Wilhelm E P, Mullen R E, Keeling P L, Singletary G W. 1999.
Heat stress during grain filling in maize: Effect on kernel
growth and metabolism. Crop Science, 39, 1733−1741.
Wu X, Chen Y Q, Sui P, Gao W S, Yan P, Tao Z Q. 2015. Effect
of planting geometries on canopy structure of spring maize
under high-density condition in North China Plain. Chinese
Journal of Ecology, 34, 1−8. (in Chinese)
Wu X M, Chen Y Q, Li Z X, Shi X P, Wang B B, Gao W S,
Sui P. 2012. Research progress of maize planting spatial
layout pattern. Journal of Maize Sciences, 20, 115−121.
(in Chinese)
Yang G P, Rhodes D, Joly R J. 1996. Effects of high temperature
on membrane stability and chlorophyll fluorescence in
glycinebetaine-deficient and glycinebetaine-containing
maize lines. Australian Journal of Plant Physiology, 23,
437−443.
Young T E, Ling J, Geisler-Lee C J, Tanguay R L, Caldwell C,
Gallie D R. 2001. Developmental and thermal regulation of
the maize heat shock protein, HSP101. Plant Physiology,
 TAO Zhi-qiang et al. Journal of Integrative Agriculture 2016, 15(12): 2677–2687
127, 777−791.
Yuan S F, Chen Y Q, Yan P, Tao Z Q, Cui J X, Li C, Sui P.
2014. Effects of water stress on growth of spring maize
and the morphological andphysiological reaction during
different growth stages in North China Plain. Journal of
China Agricultural University, 19, 22−28. (in Chinese)
Zhang A Y, Jiang M Y, Zhang J H, Tan M P, Hu X L. 2006.
Mitogen-activated protein kinase is involved in abscisic
acid-induced antioxidant defense and acts downstream
of reactive oxygen species production in leaves of maize
plants. Plant Physiology, 141, 475−497.
Zhang B R. 2003. The research on regulation and effect of
high temperature on maize yield and quality. Ph D thesis,
Shandong Agricultural University, China. (in Chinese)
Zhang J, Davies W J. 1990. Changes in the concentration of
ABA in xylem sap as a function of changing soil water status
can account for changes in leaf conductance and growth.
Plant Cell and Environment, 13, 277−285.
Zhang J W. 2005. Effects of light and temperature stress on
physiological characteristics of yield and quality in maize.
Ph D thesis, Shandong Agricultural University, China. (in
Chinese)
Zhang Z S, Li G, Gao H Y, Liu P, Yang C, Meng X L, Meng
Q W. 2013. Changes of photochemistry activity during
senescence of leaves in stay green and quick-leaf-
senescence inbred lines of maize. Acta Agronomica Sinica,
39, 93−100. (in Chinese)
2687
Zhao H F, Zhang F R, Li J, Tang H. 2008. Direction of agricultural
development of urban Beijing: Single harvest spring-maize
farming method. Chinese Journal of Eco-Agriculture, 16,
469−474. (in Chinese)
Zhao L F, Li C H, Liu T X, Wang X P, Seng S S. 2012. Effect
of high temperature during flowering on photosynthetic
characteristics and grain yield and quality of different
genotypes of maize (Zea mays L.). Scientia Agricultura
Sinica, 45, 4947−4958. (in Chinese)
Zhao Y L, Xue Z W, Guo H B, Mu X Y, Li C H. 2014. Effects
of tillage and straw returning on water consumption
characteristics and water use efficiency in the winter wheat
and summer maize rotation system. Scientia Agricultura
Sinica, 47, 3359−3371. (in Chinese)
Zheng H J, Dong S T, Wang K J, Guo Y Q, Hu C H, Zhang
J W. 2001. Effects of ecological factors on maize (Zea
mays L.) yield of different varieties and corresponding
regulative measure. Acta Agronomica Sinica, 27, 862−868.
(in Chinese)
Zhu X C, Song F B, Liu S Q. 2011. Effects of arbuscular
mycorrhizal fungus on photosynthesis and water status
of maize under high temperature stress. Plant Soil, 346,
189−199.
Zong Y Z, Wang W F, Xue Q W, Shangguan Z P. 2014.
Interactive effects of elevated CO 2 and drought on
photosynthetic capacity and PSII performance in maize.
Photosynthetica, 52, 63−70.
(Managing editor WANG Ning)