Consequences of high temperature under changing climate optima for rice pollen characteristics-concepts and perspectives

Abstract

The enhancement in both frequency and intensity of high temperature, besides its large variability will result in up to 40% yield reduction in rice by the end of 21st century. Vegetative growth in rice continues with day time temperature up to 40 °C but development of florets is extremely sensitive to temperature higher than 35 °C. The effect of night time temperature stress is even more adverse than day. Heat stress results in deprived anther dehiscence, impaired pollination and abnormal pollen germination that cause floret sterility. The decrease in pollen viability is presumably caused by imbalance in proteins expression, abandoned biosynthesis, partitioning and translocation of soluble sugars, imbalance in phytohormones release, and loss of pollen water content. Rice responds to heat stress by adjusting various physiochemical mechanisms viz., growth inhibition, leaf senescence and alteration in basic physiological processes. Antioxidant enzymes, calcium and iron also play an important role in managing heat stress. Response of rice to heat stress varies with plant ecotype, growth stage, heat intensity and time of stress application. High temperature stress can be managed by developing heat-tolerant genotypes. Rice breeding and screening may be based on anther dehiscence, pollen tube development and pollen germination on stigma.

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Consequences of high temperature under
changing climate optima for rice pollen
characteristics-concepts and perspectives
Shah Fahad, Muhammad Zahid Ihsan, Abdul Khaliq, Ihsanullah Daur, Shah
Saud, Saleh Alzamanan, Wajid Nasim, Muhammad Abdullah, Imtiaz Ali Khan,
Chao Wu, Depeng Wang & Jianliang Huang
To cite this article: Shah Fahad, Muhammad Zahid Ihsan, Abdul Khaliq, Ihsanullah Daur, Shah
Saud, Saleh Alzamanan, Wajid Nasim, Muhammad Abdullah, Imtiaz Ali Khan, Chao Wu, Depeng
Wang & Jianliang Huang (2018): Consequences of high temperature under changing climate
optima for rice pollen characteristics-concepts and perspectives, Archives of Agronomy and Soil
Science, DOI: 10.1080/03650340.2018.1443213
To link to this article: https://doi.org/10.1080/03650340.2018.1443213
Accepted author version posted online: 21
Feb 2018.
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REVIEW ARTICLE
Consequences of high temperature under changing climate
optima for rice pollen characteristics-concepts and perspectives
Shah Fahad*
a,b
, Muhammad Zahid Ihsan*
c
, Abdul Khaliq
d
, Ihsanullah Daur
e
, Shah Saud
f
,
Saleh Alzamanan
e
, Wajid Nasim
g
, Muhammad Abdullah
c
, Imtiaz Ali Khan
c
, Chao Wu
a
,
Depeng Wang
h
and Jianliang Huang
a,i
a
National Key Laboratory of Crop Genetic Improvement, MOA Key Laboratory of Crop Ecophysiology and Farming
System, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China;
b
Department
of Agronomy, The University of Swabi, Swabi Kyber Paktunkhwa, Pakistan;
c
Cholistan Institute of Desert Studies,
The Islamia University of Bahawalpur, Pakistan;
d
Department of Agronomy, University of Agriculture Faisalabad,
Pakistan;
e
Department of Arid Land Agriculture, King Abdulaziz University, Jeddah, Saudi Arabia;
f
College of
Horticulture, Northeast Agricultural University, Harbin, China;
g
Department of Environmental Sciences, COMSATS
Institute of Information Technology, Vehari, Pakistan;
h
College of Life Science, Linyi University, Linyi, China;
i
Hubei
Collaborative Innovation Center for Grain Industry, Yangtze University, Hubei, China
ABSTRACT
The enhancement in both frequency and intensity of high temperature,
besides its large variability will result in up to 40% yield reduction in rice
by the end of 21
st
century. Vegetative growth in rice continues with day
time temperature up to 40°C but development of florets is extremely
sensitive to temperature higher than 35°C. The effect of night time
temperature stress is even more adverse than day. Heat stress results
in deprived anther dehiscence, impaired pollination and abnormal pollen
germination that cause floret sterility. The decrease in pollen viability is
presumably caused by imbalance in proteins expression, abandoned
biosynthesis, partitioning and translocation of soluble sugars, imbalance
in phytohormones release, and loss of pollen water content. Rice
responds to heat stress by adjusting various physiochemical mechanisms
viz., growth inhibition, leaf senescence and alteration in basic physiolo-
gical processes. Antioxidant enzymes, calcium and iron also play an
important role in managing heat stress. Response of rice to heat stress
varies with plant ecotype, growth stage, heat intensity and time of stress
application. High temperature stress can be managed by developing
heat-tolerant genotypes. Rice breeding and screening may be based on
anther dehiscence, pollen tube development and pollen germination on
stigma.
ARTICLE HISTORY
Received 15 August 2017
Accepted 16 February 2018
KEYWORDS
Anther dehiscence; ROS;
heat stress; rice pollen
development; calcium
Introduction
Rice (Oryza sativa L.) is a primary source of food for approximately 3 billion people and accounts for
35–75% of daily calories intake, globally (Fitzgerald et al. 2009). World population is expected to rise up to
10 billion people by the end of 2050, which will exponentially increase the demand for rice in coming
decades. Globally, rice is cultivated on around 153 million hectares that accounts for 11% of the total
world arable lands (FAOSTAT 2011). Rice production is facing multiple challenges viz., extremities of water
CONTACT Jianliang Huang jhuang@mail.hzau.edu.cn National Key Laboratory of Crop Genetic Improvement, MOA
Key Laboratory of Crop Ecophysiology and Farming System, College of Plant Science and Technology, Huazhong Agricultural
University, Wuhan, Hubei, China
*These authors contributed equally to this work
ARCHIVES OF AGRONOMY AND SOIL SCIENCE, 2018
https://doi.org/10.1080/03650340.2018.1443213
© 2018 Informa UK Limited, trading as Taylor & Francis Group

stress, salinity, heat and insect pest infestation which had endangered its sustainable production (Ihsan
et al. 2014; Fahad et al. 2016a,2016b). Increase in temperature with changing climatic scenario posed a
serious threat to rice production due to its unwelcomed consequences on kernel development.
Experimental evidences have recurrently exposed the severity of short episodes of high temperature
for greater negative impacts over continuous mild stress (Schlenker and Roberts 2009). A 25-year weather
data report from International Rice Research Institute (IRRI), Philippines has indicated greater increase in
night time temperature (1.13°C) over day time temperature (0.35°C) (Peng et al. 2004). Most of the rice is
currently grown in regions where existing temperature is already close to the optimum range for rice
production. Therefore, any further rise in mean temperature or short episode of high temperature during
sensitive growth stages, will be catastrophic. A reduction of 41% in rice yield is estimated with current rate
of global temperature change by the end of 21
st
Century (Ceccarelli et al. 2010). To encounter this issue,
rice is increasingly cultivated on marginal environments thus, experiencing above-optimum temperature
stress (28/22°C) (Prasad et al. 2006; Das et al. 2014). Increase in day/night temperature above critical limits
is not uncommon in marginal environment, and hence it impaired seed set, spikelet sterility and grain
yield of rice.
Effects of heat stress vary with the duration, intensity and fluctuation of temperature above
optimal limits, and the stage of crop development (Alghabari et al. 2015)(Table 1). Likewise
other cereals, rice crop is tolerant to heat stress at vegetative stage but extremely sensitive at
reproductive stage, particularly at the anthesis stage (Jagadish et al. 2010:Ihsanetal.2016). The
temperature above 35°C at reproductive stage lasting for more than an hour resulted in
maximum spike sterility (Jagadish et al. 2007;Rangetal.2011). Irregular anther dehiscence
was the major reason for heat induced spikelet sterility. Impaired pollination and abnormal
pollen germination might be some of the other possible reasons (Matsui et al. 2005;Jagadish
et al. 2010).
Pollen quality is an important trait in determining the kernel yield and quality (Fahad et al.
2016b,2016c). Under heat stress, floral abnormalities (stamen hypoplasia and pistil hyperplasia)
lead to spikelet sterility. Major effect of heat stress during floral initiation was recorded on kernel
number. The estimated decline in kernel number with each degree increase in temperature was 4%
for temperature stress applied at 30 days preceding anthesis (Fischer 1985). Heat stress limited
photo-assimilation to the grain and increased grain filling rate with a shortening in an effective
grain filling period. Reduced endosperm cell division and elongation under heat stress has
decreased the grain plumpness (Morita et al. 2005).
Rice responds to heat stress by adjusting various physiochemical mechanisms viz., growth
inhibition, leaf rolling, leaf senescence, alteration in basic physiological processes (respiration,
photosynthesis, membrane permeability and ROS) that helps to decrease pollen sterility. Plants
experiencing heat stress at reproductive stage have to keep their male and female organs
functioning especially at meiosis stage, pollen germination, pollen tube growth, pollen-pistil
interaction, pre and post fertilization process, endosperm and embryo development (Erickson
and Markhart 2002). Rice yield reduction through decreased pollen viability is associated with
changes in several metabolites that play a significant role in pollen development by both con-
tributing to the pollen nutrition and by offering protection against heat stress (Paupière et al.
2014). Nevertheless, there is an urgent need to address high-temperature-induced pollen charac-
terizations in rice under current climatic conditions and more so in the face of a changing climate
scenario.
This review accentuates the enlarging adversities of high temperature stress and their
substantial impacts on rice pollen characteristics. Furthermore, an attempt has been made to
provide an overview of floret sterility, anther dehiscence, apical and basal pore length, pollen
fertility, pollen count per stigma, pollen germination on stigma, and pollen physiological bases.
Some strategies are also discussed for genetic improvement of rice for enhancing the tolerance
to heat stress.
2S. FAHAD ET AL.

High temperature and rice pollen characteristics
Floret sterility
Vegetative growth in rice continues with day time temperature up to 40°C but development of
florets is extremely sensitive to temperature higher than 33°C (Figure 1). Predicted global warming
has exacerbated the chances of occurrence of rice floret sterility (Matsui 2009). Booting and
flowering are considered as the most heat sensitive developmental stages in rice plant (Shah
et al. 2011; Yang et al. 2017). Temperature exceeding 35°C at anthesis stage may confer 90% floral
sterility (De Datta 1981). Deprived anther dehiscence, lower pollen production, poor pollen germi-
nation on stigma and failure to extend pollen tube are the primary causes of floret sterility (Matsui
et al. 2001; Prasad et al. 2006). The disparity in pollen germination actually occurred in those
pollens that failed to significantly accumulate iron in their pollen tubes or microspores. The
additional hypothesized explanations might be the abnormal ribosome assembly and proteins
expression specifically heat and cold shock proteins (Jagadish et al. 2010).
Influence of heat stress on floret sterility also varied among rice genotypes. A comparative
analysis of 14 rice genotypes reported cultivar difference for applied levels of heat stress depend-
ing upon their ecotype (indica and japonica) and origin (temperate and tropical) for floret sterility
Table 1. Some pronounced effects of applied high temperature stresses and durations initiated at different plant growth stages
on some pollen characteristics.
Temperature Duration Effect Plant growth stage References
Above 35/
25°C
3 days Adverse effects on panicle extrusion, spikelet anthesis,
pollen viability, pollen tube length, anther dehiscence
and pollen reception on stigma.
Panicle initiation Das et al.
2014
Above 35°C 1 h High spikelet sterility Anthesis Jagadish et al.
201038°C 5 days Heat susceptible genotypes showed only 18% spikelet
fertility. Pronounced difference was noticed in anther
length, width, apical and basal pore length.
Flowering
37°C - Resulted in 50% spikelet sterility Flowering Matsui et al.
2001
29, 33 and
36°C
< 1 h Spikelet fertility was reduced by 7% in heat susceptible
genotypes.
Anthesis Jagadish et al.
2007
38°C 48 h By increasing heat stress duration, a linear decline in
spikelet fertility was documented. Collective effect of heat
and water stress was more severe.
Anthesis Rang et al.
2011
Above 28°C // Reported decline in pollen production and pollen reception
on stigma
Flowering Prasad et al.
2006
32°C 20 DAE
until
harvest
Grains located at panicle base presented higher decline in
fertility and length compared to those on tip of panicle
// Mohammed
and Tarpley
2011
Above 37°C 6 d By increasing heat stress, tightness in locule by closure of
cell layers delayed locule opening and reduced fertility
Middle heading
stage
Matsui and
Omasa
2002
39°C/30°C 2–4 d Impaired pollen fertility and poor attachment demonstrated
partial germination on stigma
Microspore stage Endo et al.
2009
Above 32°C/
32°C
3 d Expected increase in temperature will reverse stimulatory
effect of elevated carbon dioxide on rice production in
near future
Reproductive stage Cheng et al.
2009
Above 37°C // Significantly decreased seed set Pollen germination Matsui et al.
2001
27–32°C 20 d Extent of spikelet sterility was varied from few empty
glumes to complete sterility with increasing heat stress
intensity and duration
After heading Ohe et al.
2007
35°C/30°C 2 weeks Significant variation in number of fertile spikelets, anther
length and pollen production
Before heading Inaba 2005
–10 d Documented structural abnormalities leading to premature
degeneration of tapetum. Abnormal anther development
and slower provision of metabolites to pollen resulted in
poor pollen nutrition
Anthesis Suzuki et al.,
2001
ARCHIVES OF AGRONOMY AND SOIL SCIENCE 3

(Prasad et al. 2006). Cultivar differences to applied heat stress were manifested by inconsistent
pollen production and reception on stigma that resulted in fewer filled grains and lower 1000 grain
weight (Prasad et al. 2006). A temperature stress of 35°C applied at anthesis stage even for an hour
induced floret sterility (Jagadish et al. 2010) but same stress level when applied for an hour at pre-
and post-anthesis stage failed to induce sterility (Yoshida et al. 1981). Rang et al. (2011) later on
confirmed a complete floret sterility of rice plants exposed to temperature above 35°C for 5
consecutive days at flowering stage. Effect of day time temperature of 29°C on floret sterility
were non-significant while same level of night time temperature increased rice susceptibility to
sterility and subsequently curtailed the seed set (Table 2).
Temperature effect varies among floral parts. The male gametophyte is more susceptible to heat
stress and responsible for spikelet sterility while pistil was unaffected at elevated temperature
stress (Yoshida et al. 1981). The spikelets inside the flag leaf sheath exhibited complete sterility
after high temperature stress that might be due to the extra heat trapped under leaf sheath that
limited free air flow (Das et al. 2014). Pollen grains swelling in the locules are the leading force for
anther dehiscence (Matsui et al. 1999). High temperature resulted in poor pollen grains swelling
and subsequently poor anther dehiscence (Matsui et al. 2000). Pollen grains exposed to high
temperature stress presented uniform shape but some of the important functions as pollen
adhesion and germination on the stigma were severely hindered (Endo et al. 2009). Cluster analysis
of microarray data has identified localization of some temperature responsive genes in the anther.
Expression of genes responsible for imbalance in hormonal release, abandoned biosynthesis,
partitioning and translocation of photosynthates have been ascribed the major causes for floret
sterility (Afuakwa et al. 1984). Thus, we can conclude that multiple factors contribute in florets
sterility under heat stress leading to aborted kernel production.
Figure 1. Effects of high temperature stress on young panicle growth and floret degradation at 10 days after treatments
application. (a, b) indicate young panicles of cultivar LYPJ and SY63, (c, d) indicate floret degradation in cultivar LYPJ and SY63.
ADT, high whole-day temperature treatment; CK, control; HDT, high daytime temperature treatment; HNT, high nighttime
temperature treatment (Adapted from Wu et al. 2016).
4S. FAHAD ET AL.

Table 2. Effect of different ranges of high day and tight time temperature stress on pollen characteristics.
Effect studied
Day temperature stress (°C)
References
27–30 31–34 35–38 39–42 43–46
Decrease/Increase with temperature change
Pollen tube length µm 1300 1180 - 1160 780 Das et al. 2014
Dia. of pollen grain µm 520 480 - 240 34
Pollens on stigma 37 29 - 8 2
Pollen germination % 32 12 - 6 0
Anther dehiscence % 82 46 - 20 2
Spikelet fertility % 93 - 18 - - Jagadish et al. 2010
Total number of pollen 64 - 9 - -
Germinated pollen 41 - 2 - -
Pollen tube length mm 62 - 0 - -
Anther length mm 2.19 - 2.22 - -
Anther width mm 0.68 - 0.70 - -
Basal pore area µm
2
4929 - 5992 - -
Basal pore length µm 495 - 539 - -
Apical pore area µm
2
10,318 - 12,132 - -
Apical length µm 581 - 638 - -
Stigma length mm 0.96 - 0.94 - -
Pistil length mm 2 - 2 - -
No. of anthesing spikelets 20 - 12 - - Jagadish et al. 2007
Anther dehiscence % 88 - 32 - - Rang et al. 2011
Number of germinated pollen on stigma 51 - 3 - -
Spikelet fertility % 84 - 1 - -
Pollen production (number anther
−1
) 1177 151 - - - Prasad et al. 2006
Pollen reception (number stigma
−1
) 17.6 3.8 - - -
Pollen viability (%) 92 74 - - -
Pollen viability (%) - - 76.08 - 68.70 Poli et al. 2013
Spikelet fertility (%) - - 91.00 - 69.23
Spikelet fertility (%) I 78 - - 61 - Endo et al. 2009
Spikelet fertility (%) II 78 - - 59 -
Spikelet fertility (%) III 78 - - 0 -
Spikelet fertility % 78 - 75 - - Shah et al. 2014
Grain length mm 5.47 5.48 - - - Morita et al. 2005
Grain width mm 3.12 3.05 - - -
Grain thickness mm 2.12 2.21 - - -
Endosperm cross section mm
2
5.32 5.42 - - -
Cells in endosperm 748 888 - - -
Avg. cell area (×10mm
2
cell
−1
) 717 614 - - -
Spikelet sterility% 40 - 60 - - Ohe et al. 2007
Night temperature stress (°C)
25–28 29–32 33–36 37–40 41–44
Decrease/Increase with temperature change
Spikelet fertility % - 75 10 - - Mohammed and Tarpley 2009
Pollen germination % - 30 14 - -
Spikelet sterility (%) 24 88 - - - Mohammed and Tarpley 2011
Panicle length (cm) 22.5 21.6 - - -
branches per panicle 16 17 - - -
Pollen germination % - 49 - - - Mohammed and Tarpley 2014
Spikelet fertility % 62 43 - - -
Unfilled grains Panicle
−1
38 33 - - -
Pollen germination % 58 28 - - -
Pollen germination % 30 27 - - - Mohammed and Tarpley 2011
Spikelets fertility % 78 16 - - -
Fertilized spikelet % 84 70 - - - Cheng et al. 2009
Spikelets fertility % 77 70 - - - Shah et al. 2014
Grain length mm 5.47 - 5.54 - - Morita et al. 2005
Grain width mm 3.12 - 3.00 - -
Grain thickness mm 2.12 - 2.07 - -
Endosperm cross section mm
2
5.32 - 4.84 - -
Cells in endosperm 748 - 915 - -
Avg. cell area (×10mm
2
cell
−1
) 717 - 530 - -
DAE; days after emergence, Dia; diameter, I; early panicle development, II; glumous flower primordium differentiation, III; early
microspore following meiosis
ARCHIVES OF AGRONOMY AND SOIL SCIENCE 5

Anther dehiscence
Anther dehiscence is the final step of anther development and results in the release of pollen
grains to permit pollination, fertilization and seed set. Anther is a specialized organ of the stamen
where development of the male gametophyte takes place. It consists of four maternal cell layers
i.e., epidermis, endothecium, tapetum and connective tissues surrounding the inner sporogenous
cells (Feng and Dickinson 2007).
A complex mechanism is involved in the development and release of the pollens. Cracking of
septa followed by locule wall expansion, pollen swelling and rupturing of the stomium are series of
events required for successful anther dehiscence (Liu et al. 2006). These events must synchronize
with the pollen development for the successful release of anthers and pollination (Zhu et al. 2004).
Fahad et al. (2016a) observed that both high day time (HDT) and night time temperatures (HNT)
affected the anther dehiscence of two rice varieties (IR64 and HHZ). Heat tolerant genotype HHZ
anther dehiscence was 61–54% and heat sensitive genotype IR64 was 33–22% under HDT and HNT
respectively (Figure 2). Pollen grains swelling exert pressure on anther walls that rupture and free
pollen grains (Matsui et al. 1999). High temperature treatment applied at anthesis stage increased
vapor pressure deficit thus enhanced evaporative losses from anther and thereby reduced moisture
availability required for pollen grain swelling and subsequently affected anther dehiscence that is
required for pollination (Matsui et al. 2000). A loss of 30–50% of pollen water content negatively
affected not only cell differentiation but also spikelet fertility (Liu et al. 2006).
Disparity in protein expression (dirigent and subtilisin-like proteins) is mainly responsible for
anther dehiscence under high temperature stress (Jagadish et al. 2010). These proteins play crucial
role in lignin biosynthesis to repair damaged cell wall (Johansson et al. 2000). Increased lignification
of anther walls delayed the breakdown of tissues that disturbed the regular process of anther
dehiscence.
Cultivar difference (susceptible or tolerant) for applied heat stress has been discussed for a
number of reasons. Well-developed cavities and thick locule walls in anther of tolerant cultivars
allowed easy rupture in reaction to pollen swelling and led to improved anther dehiscence and
pollen shed (Matsui et al. 2001). Heat stress not only hinders normal anther dehiscence process but
abnormal pollen developments in anther and floret deformity have been examined that headed
towards abnormal fertilization (Shi et al. 2008)(Figure 3). Usually, complete anther dehiscence
produces higher pollen interception on stigma, but in heat sensitive genotypes (Moroberekan)
even higher anther dehiscence resulted in fewer pollen reception and germination on the stigma
(Jagadish et al. 2010). Such disparity could be attributed to asynchrony between male and female
reproductive organs. Length of basal dehiscence under normal conditions is another indication for
measuring varietal tolerance to heat stress (Matsui 2005). Future research must focus on anther
dehiscence as a major trait in heat tolerant variety development programs.
Apical and basal pore length
Very little is known about the involvement of anther apical and basal pore length in pollination and
the consequent restrictions under heat stress. Basal pores are positioned just above stigmata and at
the bottom of theca, and open at the time of flower opening when the anthers stand erect.
Consequently, pollen grains in the anthers with large basal pores would readily drop out of the
basal pores on to the stigma. Significant contribution towards pollination was assessed for anther
basal pore length because of its close proximity to the stigmatic surface but knowledge regarding
apical pore length is lacking (Matsui and Kagata 2003). Thus, the basal pore length is a key
morphological trait that influences the pollen count on stigma (Matsui and Omasa 2002). Heat
stress applied for five consecutive days at flowering stage increased both apical and basal pore
length/area. Cold stress applied at anthesis stage was encountered by cold resistant genotypes
through producing bigger anthers (Suzuki 1981) and longer stigmas (Suzuki 1982) compared to
6S. FAHAD ET AL.

cold susceptible genotypes. Involvement of same morphological adaptation is considered for heat
tolerant genotypes. After successful pollination, pollen tube takes almost 30 minutes to reach
embryo sac (Cho 1956). Pollen grains with longer basal pores are readily dropped out of the pores
on the stigmata surface while anthers with smaller basal pores remain stacked to anther walls at
the time of floret splitting (Matsui and Kagata 2003). Thus apical and basal pore length along with
Figure 2. Comparison of two rice cultivars, Huanghuazhan (heat tolerant), IR-64 (heat susceptible) for different pollen
characteristics to applied high night temperature (HNT), high day temperature (HDT) and ambient temperature (AT) treat-
ments. The HDT of 35°C ± 2, HNT of 32 °C ± 2 and AT 28°C ± 2 throughout the day were provided. The HDT started at 7 am
while HNT started at 7 pm and lasted for 12 hours daily (7 pm to 7 am). Control (AT) plants were grown at 28°C (12 h-day/12
h-night cycles). The heat treatments were employed from booting stage to physiological maturity of plants. Round circles with
dashed lines indicate response curve of Huanghuazhan cultivar while triangles with dotted dashed lines represent IR-64
cultivar. Effect of HNT stress was more severe compared to HDT stress for all studied pollen characteristics for both cultivars.
ARCHIVES OF AGRONOMY AND SOIL SCIENCE 7

anther length can increase the probability of successful pollination by facilitating pollen release
under high temperature stress that decreases the chance of pollen reception and synchronization.
These traits are easy to identify, and in combination with some other traits, can be used as
breeding and screening tool for heat resistant germplasm selection.
Pollen tube growth rate vary with the susceptibility or tolerance level of genotypes under
varying intensity and duration of heat stress. For non-stressed conditions, pollen tube length of
heat susceptible (Moroberekan), medium tolerant (IR-64) and highly tolerant (N-22) genotypes
were between 1.42 mm to 1.85 mm and it was equivalent to 0.75–0.79% of the pistil length
(Jagadish et al. 2010). Under severe heat stress, susceptible genotype failed to produce pollen
germination on stigma while the pollen tube length of medium tolerant cultivar decreased up to
1.42 mm, while pollen tube length of heat tolerant genotype decreased up to 1.35 mm.
Pollen fertility
Pollen is the male gametophyte and most sensitive organ to heat stress that delivers genetic
material to embryo sac through double fertilization. Pollen is formed in the specialized organ
(stamen) that comprises of broader upper region called anther that holds pollens, and lower
stalked region containing the vasculature-the filament that extends to ensure pollen release to
stigmata surface (Goldberg et al. 1993). Mature pollen contains fructose, glucose, sucrose and
starch as major soluble sugars. Pollen is a sink for these sugars that are required for development,
growth, and protection against environmental stresses.
Figure 3. Illustration of pollen grains retained within the anthers of different cultivars under high temperature treatments.
(a–d) N22, (e–h) HHZ, (i–l) LYPJ, and (m–p) SY63. ADT, high whole-day temperature treatment; CK, control; HDT, high
daytime temperature treatment; HNT, high nighttime temperature treatment. Scale bar = 100μm (Adapted from Wu et al.
2016).
8S. FAHAD ET AL.

Tang et al. (2008) described a lower rate of pollen activity at higher temperature. Several physiolo-
gical and morphological adaptations in heat avoidance plants contribute to pollen fertility and rate of
grain setting. Heat stress sensitivity of pollens are attributed to failure of male gametophyte to respond
and produce significant quantity of heat shock proteins as compared to vegetative tissues
(Mascarenhas and Crone 1996). Pollen abortion was linked with imbalance in polyamine content
while pollen germination and pollen tube growth rate decrease was associated with spermine and
spermidine content under high temperature stress (Song et al. 2002). Endo et al. (2009) studied the
effect of heat stress (39/30°C) applied at microspore stage for 2–4 days on pollen viability. Pollen grains
displayed normal round shape when stained with Alexander reagent however, they exhibited poor
attachment and germination on the stigma surface. It was due to heat stress induced disruption in
tapetum functioning that is required for adhesion and germination on the stigma.
Heat stress caused reduction in pollen production, their release, interception, viability and
germination. Pollen quality is a crucial indicator of male fertility and health. Tapetum development
is very sensitive to heat stress. It’s a key organ that provides metabolites to the pollen. Heat
induced abnormalities in tapetum development resulted in reduced provision of metabolites to the
pollen thus displaying poor pollen nutrition. Matsui et al. (2000) connected poor pollen fertility
with the opening of anther loculi that decreased under heat stress. The effect of heat stress on
pollen fertility was dependent on several complex factors (genotype, growth stage, duration of
stress, time of stress day/night, moisture level, radiation, wind velocity and ambient recovery
conditions) that affect it individually or in an interactive way (Morita et al. 2005). Effect of heat
stress was more severe on pollens of low land genotype compared to upland genotypes. Both
quantitative and qualitative variations in pollen proteins of these genotypes were present that
possibly headed towards differential loss in viability (Jagadish et al. 2007). Nonetheless, heat stress
induced changes in physiology demonstrated adverse effects on pollen meiosis, germination, ovule
development and viability of embryo. Pressman et al. (2002) illustrated that at optimum tempera-
ture, concentration of soluble sugars gradually increased in pollen. Heat stress prevented the rise in
starch content and decreased the concentration of soluble sugars in mature pollen. The decrease in
pollen viability is presumably caused by this decrease in soluble sugars.
Pollen dehydration to increased heat intensity has been studied but information on the water
content of pollen and coping mechanism is scarce. On contrary, heat stress might have confined
soluble sugars into the locular fluid and restrict their transfer to the pollen. Low temperature stress
diluted the tapetal cell layer that led to starch-less pollen grain causing immature pollen develop-
ment (Mamun et al. 2006). Similar mechanism might be involved under high temperature stress. In
future research, there is a strong need to explore the actual mechanisms responsible for sugar
partitioning and translocation in pollens under heat stress.
Pollen count per stigma
Stigma must receive at least 20 healthy pollen grains to ensure successful pollination (Matsui and
Kagata 2003). Accordingly, half of them have to germinate on stigma. Heat stress severely
influences the number of pollens on stigma (Figure 4). Matsui et al. (2001) noted only 20% spikelet
fertility with 10 germinated pollen grains on stigma under mild stress while no fertility was noticed
at 40°C. Declined pollen reception and viability on stigma under heat stress is a direct cause of yield
reduction in rice (Fahad et al. 2015). Matsui and Omasa (2002) postulated that in heat tolerant
genotypes, larger anther size played a crucial role in inducing tolerance and compensated for the
lower number of pollen grains germinating on stigma under high temperature stress. Pollen
dispersal pattern and stickiness also contributed towards pollen reception and count on stigma.
A pollen count of less than 5, recorded 13% spikelet fertility while pollen count of more than 20
showed almost 100% spikelet fertility (Matsui et al. 1997). Although little is known about post
pollen germination processes, yet it has been reported that the processes after pollen germination
were also highly sensitive to heat stress. Liu et al. (2006) reported increased pollen stickiness that
ARCHIVES OF AGRONOMY AND SOIL SCIENCE 9

prevented pollen shedding. Relative position of style to anther and time of dehiscence to spikelet
opening were also important. Developmental escape (exposure of anther and stigma to ambient
temperature prior to pollination) was expected as a major contributor towards pollen shedding and
count on stigma under heat stress.
Pollen germination on stigma
Multiple explanations for decline in pollen germination with heat stress have been reported
previously. For instance, altered hormonal balance in the floret (Michael and Beringer 1980),
Ambient temperature High night temperature
Pollen fertilityAnther dehiscenceNo of pollen on stigma
Figure 4. Effect of high night temperature on (a) pollen fertility (b) anther dehiscence and (c) number of pollens on stigma in
rice crop (Fahad et al. 2015b).
10 S. FAHAD ET AL.

disturbance in availability of photosynthates (Afuakwa et al. 1984), lack of floral buds ability to
mobilize sugars and changes in starch biosynthesis enzymes (Keeling et al. 1994) were the main
reasons for reduced pollen germination under heat stress. Pollen germination on stigma is a
physiological factor responsible for yield reduction (Table 3). Poor germination of pollen grains
heavily caused spikelet sterility (Prasad et al. 2006). Tolerant genotype N22 presented the minimum
variation to heat stress and percentage of germinated pollen was the associated trait in this regard
(Lan et al. 2004).
Physiology of rice pollen for heat stress tolerance
Growth hormones
At high temperature stress, anther quantitative analysis displayed a decreased level of some
phytohormones (indole-acetic acid (IAA), gibberellic acid (GA
3
)), free proline and soluble proteins.
Unexpectedly, an increase was observed in abscisic acid (ABA) under heat stress (Tang et al. 2008;
Wu et al. 2016,2017; Fahad et al. 2016a). Involvement of auxin in floret sterility has been reported
by Sakata et al. (2010) as plants treated with auxin compensated for heat stress by increasing
pollen fertility over control. Auxin was supposed to alter endothecium thickening with changing
levels of heat stress. Various physiological traits such as oxidation activity, RNA content, ethylene
evolution rate, and malondialdehyde content have been reported to be involved in heat tolerance
(Zhao et al. 2018). Higher activity of roots under heat stress was due to stronger antioxidant
defense system, greater RNA content and lesser ethylene synthesis along with lower malondialde-
hyde content during meiosis (Yun-Ying et al. 2009).
Calcium and sugars
Macronutrients such as calcium (Ca
2+
) and sulfur (S) play crucial role in attaining heat stress
tolerance in plants. Calcium is known to regulate antioxidant activity rather than osmotic adjust-
ment under heat stress (Jiang and Huang 2001). Increased level of Ca
2+
modulated the heat
tempted adversities in potato crop. Kolupaev et al. (2005) reported that in heat stressed plants,
calcium improved the lipid peroxidation rate, guaiacol peroxidase, superoxide dismutase and
catalase activity. Mach (2012) reported that calcium signals might play an important role in thermo
tolerance and selection of heat tolerant varieties.
Carbohydrates availability during heat stress represents an important physiological trait asso-
ciated with high temperature stress tolerance. At low concentration sugars act as signaling
molecule while at higher concentration they become reactive oxygen species (ROS) scavenger
(Sugio et al. 2009). Normal pollen development accumulates the highest level of starch content
three days before the start of anthesis stage and, from this point onwards, converts it into soluble
Table 3. Effect of high temperature stress on rice production.
Stress level Stage of crop growth Yield reduction References
36°C whole growth period A yield reduction of 22% Ohe et al. 2007
32°C Whole growth period A decrease of 86% in grain weight Mohammed and
Tarpley 2009
32°C Reproductive A decrease of 5% in final grain yield Cheng et al. 2009
Above 33°C Heading A yield reduction of 28% Yun-Ying et al.
2009
31–39°C Early reproductive
stage
A yield reduction of 30–40% Wu et al. 2016
32°C and 35°C Booting 36% decrease in high night temperature stress and 25%
decrease in high day temperature stress
Fahad et al.
2016b
ARCHIVES OF AGRONOMY AND SOIL SCIENCE 11

sugars (Paupière et al. 2014). On contrary, in heat stressed plants, starch accumulation did not
reach to its peak and results in decreased level of soluble sugars in established pollen grains. Mild
heat stress led to a significant alteration in sugar transport, metabolism and distribution over
various anther tissues (Paupière et al. 2014). Higher activity of acid invertase also played critical role
in manufacturing hexoses under high temperature stress (Li et al. 2012). In conclusion, decreased
carbohydrates supply would have probably lowered energy flow to the pollen and subsequently
produced infertile pollens.
Calcium pretreatment increased total sugars and reducing sugars in wheat seedlings under heat
stress. While under non stress conditions, calcium has non-significant effect on acid invertase
activity. Thus, at high temperature stress, the elevated calcium might be having a role in sucrose
and starch metabolism (Bhatia and Asthir 2014). Further study is needed to explore the role of
calcium in sugar transport in developing pollens of rice crop.
Involvement of reactive oxygen species and antioxidant enzymes
High temperature exposure significantly increases ROS production in rice anther. This high
temperature induced overproduction of ROS is responsible for a decline in pollen viability and
floret fertility (Zhao et al. 2018). The increased extent of ROS concentration under high
temperature stress is extremely variable, depending upon heat intensity, duration of plant
exposure, plant growth stage and studied cultivar. At the time of pollen tube development,
pollen and tapetum cells accumulate twenty times higher mitochondria that shows faster
respiration (Selinski and Scheibe 2014). Under high temperature stress, this great amount of
accumulated mitochondria dramatically increased ROS production and suppressed the ROS
scavenging machinery (Kumar et al. 2014). Zhang et al. (2014) reported that a number of ROS
genes in rice are heat responsive. Cell keeps extensive ROS scavenging machinery to detoxify
ROS negative effects. This machinery consists of enzymes such as catalase, ascorbate peroxidase
and superoxide dismutase as well as antioxidants like ascorbic acid, flavonoids etc., (Mittler et al.
2004). The tight regulation of ROS under high temperature is very important for viable pollen
production. Exogenous application of antioxidants may increase pollen viability under heat
stress by ROS scavenging (Fahad et al. 2016a).
Genetic basis for heat stress tolerance
Clustering of microarray data has identified various genes responsible for heat stress tolerance in
rice crop. Among these studied genes, thirteen were localized in the anther. Expression analysis has
revealed that these genes were specifically expressed in immature anthers especially in tapetum at
microspore stage and a minimum of 24 hours of heat stress was required to down regulate these
tissue specific genes (Endo et al. 2009). The tapetum specific genes (Osc6, OsRAFTIN and TDR) were
unaffected to long exposure of heat stress. This indicates the inhibition of selective genes by the
heat stress. Gene ontological studies revealed an impaired activity of genes important for pollen
development under heat stress. Minor reduction in functionality was noted after 3 and 4 days of
applied stress. It further confirmed that not all genes were involved in down-regulation/degrada-
tion of tapetum except for some specific ones (Endo et al. 2009).
Cellular membranes are primarily composed of proteins and lipids. Disorganization in lipid and
protein content in matured pollen were studied to applied levels of heat stress that influenced
membrane structure, integrity and pollen viability (Das et al. 2014). Two of the genes, expressed in
tapetal cells, were suppressed by heat stress indicating the involvement in lipid metabolism. The
plant specific c cytochrome P450 (CYP703) was an expression of gene AK106843 while AK106946
encoded a GDSL lipase. The CYP703 catalyzed the conversion of saturated fatty acid and has major
part in sporopollenin synthesis (Morant et al. 2007). Mayfield et al. (2001) reported GDSL involve-
ment in pollen coat formation in A. thaliana. The exact biological activity in rice anther of these two
12 S. FAHAD ET AL.

genes is still unclear. The possible mechanism may include heat induced alteration in the pollen
wall lipid composition.
Conclusions and future prospective
High temperature stress is the major upcoming challenge for successful rice production. The
adversity of the effect depends upon crop growth stage, duration and intensity of the applied
stress. Pollen is more heat sensitive over stigma. Therefore, understanding and management of
anthesis stage is vital for rice heat tolerance. The responses of rice plant to heat stress have been
studied intensively in recent years; however, a complete understanding of thermo tolerance
mechanisms remains elusive. The role of osmoprotectants and phytohormones also remains
unclear under mild and extreme heat stress conditions. A little progress has been made in
developing heat tolerant genotypes through traditional breeding and genetic engineering
approaches. The above discussed rice pollen characteristics can be exploited as screening tools
for varietal development but selection must focus for those germplasm sources which can tolerate
temperature above 38°C.
Further study is needed to find out the physiological basis of osmotic adjustment, assimilate
partitioning and protein denaturation for heat stress tolerance. Exact role of sugars and calcium in
pollen fertility needs to be studied in detail. Involvement of roots in heat stress management and
root-shoot signaling mechanisms also needed exploration in future research. Knowledge at mole-
cular level about heat tolerance mechanisms will pave the ways for engineering plants that can
tolerate heat stress and might be the source for crop production under heat stress conditions. For
better understanding of plant heat stress tolerance, application of genomics, proteomics and
trascriptomics is imperative.
Acknowledgments
We thank the funding provided by the Major International Joint Research Project of NSFC (No. 31361140368).
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This work was supported by the Major International Joint Research Project of NSFC [31361140368];
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