Plant Breeding
12217
2014 Blackwell Verlag GmbH
Review
Heat stress in crop plants: its nature, impacts and integrated breeding strategies
to improve heat tolerance
U D A Y C H A N D J H A 1, A B H I S H E K B O H R A 1 and N A R E N D R A P R A T A P S I N G H
Indian Institute of Pulses Research (IIPR), Kanpur, 208024, India; 1Co-Corresponding authors, E-mail: uday_gene@yahoo.co.in and
abhi.omics@gmail.com
With 1 figure and 3 tables
Received April 2, 2014 / Accepted August 25, 2014
Communicated by R. Tuberosa
Abstract
Increasing severity of high temperature worldwide presents an alarming
threat to the humankind. As evident by massive yield losses in various
food crops, the escalating adverse impacts of heat stress (HS) are putting
the global food as well as nutritional security at great risk. Intrinsically,
plants respond to high temperature stress by triggering a cascade of
events and adapt by switching on numerous stress-responsive genes.
However, the complex and poorly understood mechanism of heat toler-
ance (HT), limited access to the precise phenotyping techniques, and
above all, the substantial G 9 E effects offer major bottlenecks to the
progress of breeding for improving HT. Therefore, focus should be given
to assess the crop diversity, and targeting the adaptive/morpho-physiolog-
ical traits while making selections. Equally important is the rapid and
precise introgression of the HT-related gene(s)/QTLs to the heat-suscepti-
ble cultivars to recover the genotypes with enhanced HT. Therefore, the
progressive tailoring of the heat-tolerant genotypes demands a rational
integration of molecular breeding, functional genomics and transgenic
technologies reinforced with the next-generation phenomics facilities.
Key words: heat stress tolerance genomics molecular
markers QTL
The global climate will witness an increase of 24C tempera-
ture at the end of 21st century (IPCC 2007). More importantly,
the predictions based on global climate model analysis suggest
that the tropical and subtropical regions of the world will be the
worst sufferer from the forthcoming disaster of heat stress (HS)
(Battisti and Naylor 2009). Lobell and Gourdji (2012) have
reported linear trends in increase in average maximum and mini-
mum temperatures per decade (19802011) with average of
0.3C Tmax and 0.2C Tmin, respectively. As a consequence of
increase in temperature, alterations in plant phenologies such as
spring and autumn phenologies were noticed across different
plant species and also within plant species (Ib
a~nez et al. 2010,
Li et al. 2014a). In particular, the earliest flowering species in
spring are the most sensitive to high temperature (Wolkovich
et al. 2012). Therefore, increasing HS in various crop species is
emerging as an alarming issue especially in concern to the global
food security. In response to HS, plants are endowed with differ-
ent mechanisms and regulatory networks, viz. regulating vital
genes, managing numerous physiological and biochemical adap-
tations and so forth. The complex genetic structure of heat toler-
ance (HT) offers a great challenge to breeders (Blum 1986),
which is further exacerbated by the presence of large magnitude
of G 9 E and epistatic interactions (Cossani and Reynolds
2012). This article highlights the enlarging adversities of HS and
their substantial impacts on crops that have been seen in the
doi:10.1111/pbr.
recent past. Further, an attempt has been made to provide an
overview on underlying mechanism that includes heat signal per-
ception crosstalk, and role of heat-shock proteins (HSPs) and
transcription factors (TFs). Finally, we discuss optimizing breed-
ing strategies that focus on efficient utilization of germplasm
resources and existing genetic variability together with exploring
the future scope for integrating a wide range of emerging for-
ward and reverse genetic techniques, and the phenomics plat-
forms.
Crop Yield Losses Due to HS: Retrospect and Future
Projections
Region-wise overview on crop losses
The unprecedented rise in temperature extremities in the last dec-
ades revealed a broad range of anomalies associated with HS. Its
severe impacts on various crops have been demonstrably evident
in different parts of the world. In Yangtze River Valley (YRV),
the pivotal rice-growing area of China repeatedly (six times)
faced HS, causing severe loss of mid-season rice (Tian et al.
2009). The prolonged HS resulted in poor seed set (up to 10%
only) in heat-susceptible rice genotypes and hybrids in Hubei
and Sichuan provinces of China, leading to severe loss in rice
production (Tian et al. 2009). Similarly, by analysing data from
1979 to 2000, You et al. (2009) noted up to 10% reduction in
wheat yield, which could be credited to 1C temperature increase
during wheat-growing season in China. Taken recent trends into
consideration, it is envisaged that India will lose 0.45 tons/ha,
while China will encounter a 47% reduction in rainfed wheat
yields, which would be attributable to a rise of 0.5C in average
temperature by 2050 (Easterling et al. 2007). Manigbas and
Sebastian (2007) have reported that the high temperature (38.0
39.9C) during mid-April to early May in major rice-growing
areas in Philippines (particularly central and northern parts of
Luzon) renders these regions more vulnerable to HS.
Several research groups (Chatrath et al. 2007, Joshi et al.
2007a, Singh et al. 2007a) have highlighted the increasing vulner-
ability of the major wheat-growing areas to HS. The likely
vulnerable regions include South Asia that covers Eastern Ganget-
ic Plains (EGP), central and peninsular India and Bangladesh. By
2050, Indo Gangetic Plain (IGP) of mega environment-1 (ME1),
which accounts for almost 15% of the global wheat production,
will be redefined as heat-stressed, irrigated and short-season pro-
duction mega environment (Ortiz et al. 2008). Moreover, Gupta
et al. (2012) pointed out that the five MEs (ME4, ME5, ME6,
ME9 and ME12) under wheat cultivation are inflicted due to HS
2 U. C. JHA, A. BOHRA,
and shortage of water. Similarly, climatic model analysis delin-
eates central and eastern Asia, central North America and northern
part of Indian subcontinent as the major HS-prone regions for
growing wheat, maize, rice and soybean (Teixeira et al. 2013).
Further, it is reported by the Working Group II of IPCC that India
would likely to suffer from 10 to 40% loss in crop production due
to HS by 20802100 (see Aggarwal 2008).
As a result of abnormal rise in July temperatures (6C above
the long-term means) coupled with the occurrence of scanty rain-
fall, Europe faced the hottest summer in 2003 and witnessed
record losses in crop yield (Stott et al. 2004, Ciais et al. 2005).
Likewise, adverse effects of increasing temperature on crop yield
are likely to reflect in Pannonian zone encompassing Hungary,
Serbia, Bulgaria and Romania (Olesen et al. 2011). Recently,
noticeable reduction in maize yield was recorded in France due
to maximum temperature rising beyond 32C each day (Hawkins
et al. 2013). Similarly, dry and hot summer causing shrinkage
of maturity period in European wheat-growing regions are also
experiencing marked deterioration in yield (Semenov et al.
2014). Furthermore, given the ever-expanding severity of HS,
whole Europe will likely to face substantial crop losses not pri-
marily due to drought but because of increasing incidence of HS
(Semenov and Shewry 2011).
In Africa, analysis of historical data covering more than
20 000 maize trials suggested 1% and 1.7% yield losses under
rainfed and drought conditions, respectively, due to rise of each
one degree temperature beyond 30C (Lobell et al. 2011a).
Similarly, reclassification of new maize MEs is anticipated, and
more importantly, maize MEs within sub-Saharan Africa region
are envisioned to encounter severe threat of temperature rising
by 2.1C (Cairns et al. 2012, 2013a).
Future yield reductions of 13% and 16% in corn and soybean,
respectively, were indicated by analysing the patterns of temper-
ature change in USA during 19762006 (Kucharik and Serbin
2008). Likewise, Southern plains and south-west regions of the
United States suffered sizeable agricultural loss estimating US$5
billion owing to combined drought and HS (NCDC 2011). Lo-
bell et al. (2013) suggested that the rise in temperature beyond
30C would exert noteworthy negative impacts in rainfed maize
in USA and Africa.
Crop-wise impact of HS worldwide
Substantial reductions in yield were documented in various
important food crops worldwide (Lobell and Field 2007, Lobell
et al. 2008). For instance, massive yield loss of 5.18 million tons
was reported from 3 million ha area in China in rice due to the
disastrous HS episode of 2003 (Li et al. 2004, Tian et al. 2009).
Similarly, Lobell et al. (2008) recorded 414% yield loss in rice
due to 1C increase in temperature in South-East Asia.
In addition to rice, Reynolds et al. (2001) asserted that seven
million hectares in developing countries as well as 36 million ha
in temperate environments representing the prominent wheat-
growing areas are likely to be severely hit by HS. Similarly, Lo-
bell and Field (2007) reported an annual global yield reduction
of 19 million tons in wheat, costing $2.6 billion, due to unusual
warming during 19812002. According to a report published by
USDA (2010), nearly 30% of the total wheat production was
reduced in Russia, which was attributable to drought and HS.
Worldwide, temperature trend analysis (19802008) has shown
about 5.5% reduction in wheat production (Lobell et al. 2011b).
Recently, based on 9 years satellite data on wheat growth in
northern India, Lobell et al. (2012a) suggested that temperature
AND N. P. SINGH
above 34C increases the rate of senescence, thereby causing
significant loss in grain yield.
In case of maize, warming between 1981 and 2002 has
accounted losses up to 12 million tons per year comparable to a
monetary loss of $1.2 billion (Lobell and Field 2007). In a similar
study, up to 10% reduction in maize yield was recorded due to
increase in temperature (6C) during the grain-filling stage (Thom-
son 1966). More severe maize yield reductions have been pro-
jected in USA by Kucharik and Serbin (2008) based on the
patterns of temperature change that were observed in USA during
19762006. By 2100, yield loss of 30% in corn was predicted in
USA using the nonlinear and asymmetric temperature and yield
relationship analysis (Schlenker and Roberts 2009). A 3.8% reduc-
tion in maize production was shown by global temperature trend
analysis using historical yield data from 1980 to 2008 (Lobell
et al. 2011b). Similarly, Lobell et al. (2013) observed that rise of
temperature beyond 30C will cause negative impacts in rainfed
maize in USA and Africa. Additionally, Deryng et al. (2014) have
suggested that extreme HS at anthesis could potentially decrease
45% of the global maize yield by 2080s as compared to 1980s.
In soybean, nonlinear and asymmetric temperature and yield
relationship analysis has predicted almost 46% yield loss in
USA before year 2100 (Schlenker and Roberts 2009). Future
yield reduction of 16% has been indicated in soybean based on
the patterns of temperature change prevailed in USA during
19762006 (Kucharik and Serbin 2008). Similarly in barley,
warming from 1981 to 2002 caused loss of eight million tons
per year, costing around $1.0 billion (Lobell and Field 2007).
Therefore, given the burgeoning agricultural adversities and
increasing evidences of negative impact of HS on crops world-
wide, an immediate attention is needed to transform breeding
strategies and to reconstruct crop ideotypes followed by an in
silico testing using simulation models (Gupta et al. 2012, Seme-
nov and Stratonvitch 2013).
HS in Crops: Influencing Plants from Germination to
Maturity
A series of in-depth reviews were published in recent years
describing the detrimental impacts of HS on crop growth and
development (Wahid et al. 2007, Bita and Gerats 2013, Hasa-
nuzzaman et al. 2013). High temperature stress impairs various
vital physiological processes in plants, including photosynthesis,
respiration and transpiration through impeding carbon assimila-
tion (Stone 2001). The stress-led alterations in plants physiology
hinder the overall reproductive processes and eventually result in
substantial yield loss (Barnab
as et al. 2008, Hedhly et al. 2008,
Zinn et al. 2010).
Impacts of HS on warm-season crops
Considering impacts on warm-season crops, rice is among the
major food crops that often encounter the challenges of increas-
ing HS in tropical and subtropical regions, especially South and
South-East Asia (Jagadish et al. 2012, Manigbas et al. 2014).
Escalating HS has raised a serious concern in major rice-growing
areas of Asia (Catherine and Gemma 2012). In rice, HS impedes
various stages starting from the emergence to the harvesting
(Krishnan et al. 2011, Shah et al. 2011). Temperature beyond
40C strictly restricts the emergence of rice seedlings (Yoshida
et al. 1981, Akman 2009). Simulation studies have shown a
10% reduction in rice yield with rise of each 1C minimum tem-
perature during growing periods (Peng et al. 2004). In a similar
Heat stress in crop plants
way, Lyman et al. (2013) have also observed a 6.7% reduction
in rice yield, which is attributable to an average 1C rise in tem-
perature during the growing period. Several attributes such as
plant height, tiller number and total dry weight were known to
be affected negatively by temperature rising beyond 32C/25C
(Yoshida et al. 1981).
Concerning differential susceptibility of various growth phases
to HS, flowering stage and microsporogenesis were reported to
be the most vulnerable in rice (Satake and Yoshida 1978,
Nakagawa et al. 2002). Subjecting rice to 41C temperature for
4 h at flowering stage resulted in the complete sterility (IRRI
1976). Likewise, spikelet sterility was noted at temperatures ris-
ing beyond 33C, and notably, most of the grains showed empti-
ness above 35C (Matsui et al. 1997, 2000, Jagadish et al.
2007). In case of maize, impaired protein synthesis in embryo
led to the inhibition of germination at temperatures beyond 37C
(Riley et al. 1981). The coleoptile growth is completely halted
in maize at 45C (Weaich et al. 1996, Akman 2009). Similarly,
HS leads to an enhancement in respiration and reduction in pho-
tosynthesis in maize (Crafts-Brander and Salvucci 2002), which
often causes pollen sterility and inflicts kernel development
(Schoper et al. 1987a,b, Cheikh and Jones 1994).
Instances are reported in soybean, where prevalence of HS dur-
ing seed filling stage caused lowering in germination and seedling
vigour (Egli et al. 2005). Under tropical humid conditions,
increase in temperature above 30C impoverished seed production
in soybean (Lindsey and Thomson 2012). Negative impact of high
temperature on growth and photosynthesis in different legumes
was also documented by McDonald and Paulsen (1997). For
example, temperature above 30C hampers microsporogenesis in
common bean (Porch and Jahn 2001, Rainey and Griffiths 2005,
Porch 2006). A wide range of reproductive traits from pollen via-
bility to fertilization process including pod and seed setting were
investigated in common bean (Anthony et al. 1980, Weaver and
Timm 1988, Gross and Kigel 1994) and groundnut (Prasad et al.
1998, 1999a,b, 2000, 2001). Apart from legumes, demonstrably
reliable evidences were also gained in other important crops such
as sorghum (Eastin et al. 1983, Prasad et al. 2008) and cotton
(Singh et al. 2007b). In sorghum, failure of germination and epi-
cotyl emergence was reported due to soil seed zone temperature
exceeding 45C (Peacock et al. 1993). Likewise, cessation of
seedling emergence was noticed beyond 30C in tomato (Camejo
et al. 2005). Additionally, HS diminishes net photosynthetic rate
(Camejo et al. 2005), pollen grains and their viability (Pressman
et al. 2002) and ultimately impairs the fruit development (Peet
et al. 1998, Adams et al. 2001).
Impact of HS on cool-season crops
With regard to cool-season crop, more than 13.5 million ha of
wheat-growing area in India is under HS (Joshi et al. 2007a,b).
Given increasing severity during heading to maturity, HS is
becoming a major concern in cooler northern wheat-growing
regions (Liu et al. 2014). Joshi et al. (2007a) and Singh et al.
(2007a) reported Eastern Gangetic Plains (EGP), central and pen-
insular India and Bangladesh as the most vulnerable regions to
HS in South Asia for growing wheat. Severe damages due to HS
were also noted in late-sowing wheat, in particular during grain-
filling stage (Rane et al. 2007). Joshi et al. (2007a) and Rane
et al. (2007) reported that curtailing cool period in wheat also
resulted in yield reduction. Likewise, Asseng et al. (2011) specu-
lated that temperature variation of
2 C during growing season
could potentially reduce 50% yield in Australia. HS impairs seed
3
germination in wheat by disrupting the function of enzymes that
are associated with starch breakdown (Essemine et al. 2010).
Concerning flowering period, key determining stages involving
grain size and grain number development, and ultimately the
yield represent the most vulnerable stages in wheat (Semenov
2009, Farooq et al. 2011). Various abnormalities were observed
in wheat that could be ascribed to HS, which include unusual
ovary development (Saini et al. 1983), tapetum degradation dur-
ing microspore meiosis and pollen sterility (Saini et al. 1984,
Sakata et al. 2000, Zinn et al. 2010), disruption in starch synthe-
sis during early grain-filling period and lowering in biomass pro-
duction (Reynolds et al. 2007). In case of cool-season legumes,
germination rates of chickpea and lentil seeds are retarded owing
to increase in temperature above 33 and 24.4C, respectively
(Covell et al.1986), while anomalies were manifested with soil
temperature above 32C in lettuce (Gray 1975). Several investi-
gations describing growth retardation, and adverse impact on
photosynthesis in Brassica juncea L. (Hayat et al. 2009) and
inflicted seed production due to hindrance in micro- and mega-
gametophyte fertility in B. napus were noted under HS (Young
et al. 2004).
Molecular Mechanism Underlying HS Acclimation
Stimuli of abiotic stress perceived by the plant generate an inte-
grated signalling cascade that is generally triggered by receptors
embedded in plasma membrane of the cell (Vigh et al. 1998,
Sangwan et al. 2002, Los and Murata 2004). Secondary messen-
gers such as Ca2+ ion and calmodulins (Liu et al. 2003, Wu and
Jinn 2010), calcium-dependent protein kinases (CDPKs), calci-
neurin B-like (CBL) (Das and Pandey 2010) and CBL-interacting
protein kinases (CIPKs) (Kolukisaoglu et al. 2004) act as calcium
sensor. This event switches the mitogen-activated protein (MAP)
kinases on, followed by the activation of transcription factors and
subsequently the concerned heat-shock protein (HSP) genes
(Sangwan et al. 2002, Suri and Dhindsa 2008). The complex
pathway underlying HS perception and signal transduction are
described in detail elsewhere (Larkindale and Knight 2002, Sung
et al. 2003, Kaur and Gupta 2005, Saidi et al. 2010).
While confronting high temperature stress and alleviation from
damage of cellular protein structure essential for survival in
stressed conditions, plant triggers a novel class of protein called
HSPs. These HSPs serve as molecular chaperons to maintain
conformational protein functions as well as cellular protein
refolding, thereby protecting plants under HS conditions (Bani-
wal et al. 2003, Wang et al. 2004).
Based on molecular weight, function and amino acid
sequence, the HSPs can be categorized into five major types,
viz. Hsp100, Hsp90, Hsp70, Hsp60 and sHSPs (Schlesinger
1990, Schoffl et al. 1998, Kotak et al. 2007, Gupta et al. 2010a,
b, Al-Whaibi 2011). Higher plants generate HSPs as and when
these are subject to HS conditions (Vierling 1991). In response
to extreme environmental stresses, plant expresses stress-respon-
sive genes that are regulated by numerous TFs via binding to
the cis-acting promoter of the concerned gene (Nakashima et al.
2009, Zhang et al. 2009a, Dubos et al. 2010, Chen et al. 2012a,
Mizoi et al. 2012).
Harnessing Crop Germplasm Repertoire for Breeding
Against HS
Keeping yield as the principal criterion, serious breeding efforts
were made to develop high-yielding cultivars in most of the
4 U. C. JHA, A. BOHRA,
important food crops. The conventional crop breeding schemes
relying solely on selection and intermating have unintentionally
resulted in paucity in the genetic variation especially for eco-
nomically important traits that underwent domestication/selection
(Tanksley and McCouch 1997, Eyre-Walker et al. 1998, Lee
1998, Gur and Zamir 2004, McCouch 2004). Therefore, acceler-
ating crop improvement demands an extensive search for genetic
variability in cultivated as well as in wild species. In the context,
heat-tolerant gene(s)/QTLs and the component traits conferring
HT must be explored thoroughly within the entire gene pool,
especially targeting the non-adapted and underutilized crop wild
relatives (CWRs) and the landraces (Lee 1998, Fernie et al.
2006). Impressive accomplishments were achieved in harnessing
the natural genetic variation for HT, and additional efforts are
underway to introduce the heat-tolerant QTLs/genes into differ-
ent genetic backgrounds (Jagadish et al. 2008, Jiang-lin et al.
2011). The presence of HT was examined in cultivars and wild
species of wheat (Rawson 1986, Edhaie and Waines 1992,
Reynolds et al. 1994a). Similarly, a rice wild relative (Oryza me-
ridionalis) exhibited higher growth rate and less affected photo-
synthesis at 45C compared to O. sativa ssp. japonica (Scafaro
et al. 2010). Two rice genotypes, viz. Dular and Todorokiw-
ase, offered higher HS tolerance at booting stage at 39C, while
Milyang 23 showed tolerance at flowering stage at 38C (Ton-
orio et al. 2013). On the other hand, tolerance was manifested at
both the above-mentioned stages by Giza 178. Jagadish et al.
(2008) reported advantages offered by the genotype CG14
(O. glaberrima) that reached peak anthesis stage earlier than
O. sativa under both controlled and HS conditions. In addition,
they also noted that the cultivar N22 possessed marked HS tol-
erance (Jagadish et al. 2010a,b, Madan et al. 2012) exhibiting
6486% spikelet fertility at 38C temperature compared to the
susceptible cultivars, viz. Azucena and Moroberekan, that had
meagre fertility (up to 8%) (Jagadish et al. 2008). Later, higher
pollen viability and spike fertility under HS were confirmed in
rice genotypes, viz. N22 and NH219 (Poli et al. 2013). In
recent past, introgression breeding in rice facilitated transfer of
HT from N22 to Xieqingzao B line by developing BC1F8
lines (Jiang-lin et al. 2011). Additionally, advanced line derived
from Gayabyeo/N22 cross has offered HS tolerance and high
yield (Manigbas et al. 2014). Given the importance of anther
dehiscence in imparting HS tolerance, a study was undertaken in
rice to evaluate anther characteristic, especially closure of locules
under high temperature (Matsui and Omasa 2002). Consequently,
japonica rice cultivars Nipponbare and Akitakomachi exhib-
ited higher fertility under 37.5C/26C temperature during flow-
ering (Matsui and Omasa 2002).
In wheat, wide variation was revealed in the wild progenitor
Aegilops tauschii Coss. in comparison with the tolerant cultivar
C273 for important HT-related traits such as cell membrane
stability and TTC (2, 3, 5-triphenyl tetrazolium chloride)-based
cell viability (Gupta et al. 2010b). Recently, A. tauschii was suc-
cessfully used as a donor for incorporating HT-relevant compo-
nent traits such as cell membrane stability and chlorophyll
retention into cultivar PBW550 through backcrossing (Sehgal
et al. 2011). Likewise, identification of A. speltoides Tausch and
A. geniculata Roth species offering HS tolerance at reproductive
stage opens up new opportunities for incorporation of HT genes
in hexaploid wheat in near future (Pradhan et al. 2012a). By
screening wheat against stressed conditions involving both
drought and HS, ALTAR 84/AOS and ALTAR 84/A. tauschii
genotypes remained least affected, notably at two critical stages:
(i) from emergence to anthesis and (ii) from emergence to post-
AND N. P. SINGH
anthesis (another 21 days after anthesis) (Pradhan et al. 2012b).
More recently, attempts were made in wheat aiming at introgres-
sion of wheat-Leymus racemosus chromosome to Chinese
spring cultivar to enhance HT and better adaptation under HS
(Mohammed et al. 2014). In search of some novel sources for
HT, Hede et al. (1999) explored potential of wheat landraces,
and consequently, three Mexican landraces were identified that
carried superior canopy temperature depression trait. Further,
concerning germination-related traits, two genotypes, viz.
Moomal-2000 and Mehran-89, performed better at 2030 C
(Buriro et al. 2011). Recently, while investigating photosynthetic
activity in flag leaves during grain-filling stage, Feng et al.
(2014) identified cultivar Jimai22 having 6% less reduction in
grain yield under HS. Additionally, this cultivar also offered
benefits including stability of PSII and carboxylation activity
under HS. Evaluation at terminal growth stage focusing stay
green trait resulted in the discovery of three promising genotypes
on the basis of maximum grain development and higher survival
under stressed conditions (Rehman et al. 2009). More recently,
promising genotypes WH1021 and WH730 showing
enhanced yield under HS were discovered in wheat (Dhanda and
Munjal 2012). In the same way, three synthetic wheat lines, viz.
SYN 11, SYN36 and SYN44, were declared as highly tolerant
to heat based on cluster analysis of morphological attributes and
ISSR markers (Sharma et al. 2014a).
In case of tropical grain legumes, direct selection targeting
yield led to the recovery of a tolerant genotype California
Blackeye No. 27 (CB27) characterized by the tolerance to HS
at reproductive stage (Ehlers et al. 2000). In parallel, two
additional genotypes B89-200 and TN88-63 also showed
higher yield under hot short days (Ehlers and Hall 1998). Like-
wise, four common bean genotypes, viz. SRC-1-12-1-182,
SRC-1-12-1-48, 98020-3-1-7-2 and 98012-3-1-2-1, were
found to be tolerant to HS on the basis of stress indices such as
heat tolerance index (HTI), heat susceptibility index (HSI) and
geometric mean (GM) analyses (Porch 2006). In chickpea, HS-
tolerant genotype ICCV 92944 was identified while screening
diverse genotypes under field conditions (Gaur et al. 2012). Sev-
eral other chickpea genotypes with enhanced HT are listed
recently by Jha et al. (2014). Pollen-based screening of geno-
types delivered various tolerant accessions in different crop spe-
cies. Examples include DG 5630RR in soybean (Salem et al.
2007), AZ100 in maize (Petolino et al. 1992) and ICC1205
and ICC15614 in chickpea (Devasirvatham et al. 2012, 2013).
Recently, La Posta Sequia C7-F64-2-6-2-2 and DTPYC9-F46-
1-2-1-2 were identified in maize carrying tolerance to both
stresses, that is, drought and heat (Cairns et al. 2013b).
Apart from the genotypes described above, several hybrids
including YH-1898, KJ. Surabhi, FH-793 ND-6339 and
NK -64017 provided stable yield under HS (Rahman et al.
2013). Important cultivars of tomato Fresh market 9, Sala-
dette, Processor 40 and Solar set have been reported to set
fruit under HS (Abdul-Baki 1991).
Heat escape means an alternative mechanism through which
plant completes its life cycle before the onset of HS. This prop-
erty has been exploited in developing early maturing genotypes
in durum wheat such as Waha-1, Omrabi-5 and Massara-1
(Al-Karaki 2011). By using temperature induction response
(TIR) technique, Senthil-Kumar et al. (2003) observed adequate
genetic variability for thermotolerance among the parental lines
of the hybrid KBSH-1, viz. CMS234A, CMS234B and
6D-1. In a similar manner, application of chlorophyll fluores-
cence measurement techniques in USDA upland cotton collec-
Heat stress in crop plants
tion resulted in the identification of nine wild accessions with
high vegetative HT (Wu et al. 2013). The availability of poten-
tial donors for HT would encourage plant breeders not only to
deploy these novel sources directly in breeding schemes but also
to excavate the resilient alleles that underlie tolerance.
Physiological and Adaptive Trait Breeding for HS
Tolerance
Concerning yield improvement under stressed conditions, several
factors such as low heritability and a complex network of major
and minor QTLs limit the efficacy of direct selection method
(Hittalmani et al. 2002, Leung 2008, Manavalan et al. 2009).
Compounding the problem, environmental factors present addi-
tional barriers to breeding for high-yielding lines with enhanced
HT. Furthermore, poor understanding of genetic inheritance of
heat coupled with less availability of validated QTLs/cloned
gene(s) for HS tolerance in plants limits the progress of crop
improvement (Cossani and Reynolds 2012). Given the context,
genetic tailoring of the physiological traits could be a promising
approach for incorporating gene(s)/QTLs that determine complex
abiotic stress tolerance in crop plant. Physiological trait-based
breeding strategy provides advantage over conventional breeding
approach (Reynolds and Trethown 2007). Additionally, physio-
logical approach offers the benefit of maximizing the probability
to harness the more relevant additive gene actions (Reynolds
and Trethown 2007). Extensive efforts were undertaken for
physiological trait breeding in wheat at International Maize and
Wheat Improvement Center (CIMMYT), which primarily relied
on three basic steps: i) characterization of the parental genotypes
in various crossing schemes; ii) appropriate mating scheme
designed to target traits; and iii) selection of superior progeny
from the early generations (Reynolds et al. 2009).
Central to the HS acclimation, breeding should be aimed at
physiological traits that are related to canopy structure, delayed
senescence, photosynthesis efficiency, less respiration rates,
reproductive traits and the harvest index (Cossani and Reynolds
2012, Gupta et al. 2012). As evident from the above description,
emphasis should be given to capture the genetic variation in
plant phenologies that confers better adaptation under stressed
conditions (Evans 1993). In parallel, selection for morpho-physi-
ological traits that are involved in drought acclimation and indi-
rectly associated with yield constitutes an alternative approach
for enhancing drought tolerance in crop plants (Richards 1996,
Tuberosa et al. 2002). The potentiality of this approach for
enhancing HT was explored in wheat (Cossani and Reynolds
2012). Substantial genetic variability for photosynthetic rate
under HS was detected in wheat (Blum 1986, Delgado et al.
1994). Similarly, the genetic variability was evaluated by sub-
jecting 16 wheat genotypes to HS at CIMMYT (Reynolds et al.
2000). Likewise, high level of photosynthetic rate in leaves was
demonstrated to serve as a potential indicator of HS tolerance in
rice (Restrepo-Diaz and Garces-Varon 2013). The genetic vari-
ability resulted from loss of chlorophyll content and premature
leaf senescence (Al-Khatib and Paulsen 1984, Harding et al.
1990). In a likely manner, three HS-tolerant landraces were iden-
tified in wheat by evaluating leaf chlorophyll content (LCC),
canopy temperature depression (CTD) and thousand-kernel
weight (KWT) (Hede et al. 1999). While screening over 1000
wheat genotypes, the chlorophyll fluorescence was established as
an important physiological parameter (Sharma et al. 2012).
Apparently, CTD could be considered as the potential
mechanism underlying heat escape in cotton (Cornish et al.
5
1991), and it is also demonstrated to be an effective selection
parameter against HS in wheat (Amani et al. 1996, Fischer et al.
1998).
Considerable extent of phenotypic variation (PV) was noticed
in wheat (Pierre et al. 2010), and meaningful conclusions were
generated suggesting correlation of CTD value with HT in wheat
(Balota et al. 2008, Pradhan et al. 2012b). Similarly, the cooler
canopy temperature (CT) caused higher yield under HS in wheat
(Kumari et al. 2012, Mondal et al. 2013). Reynolds et al.
(1994a) experimentally demonstrated that CTD in conjunction
with flag leaf stomatal conductance and photosynthetic rate is
positively correlated with yield in wheat under HS. Blum and
Ebercon (1981) surveyed the genetic variation for membrane
thermostability (MT) in different crops and advocated that MT
under HS should be considered as a vital component for measur-
ing HT. Practicing selection under HS for MT during anthesis
stage delivered significant yield improvements in wheat (Shana-
han et al. 1990). Various physiological traits and their relative
contributions to HT in wheat are discussed in detail by Gupta
et al. (2012).
Screening against HS based on parameters such as electrolyte
leakage from cell membrane and chlorophyll fluorescence
revealed negative association of membrane injury with specific
leaf weight in some legume species including groundnut and
soybean (Srinivasan et al. 1996). Combination of the two selec-
tion parameters, viz. high chlorophyll content and MT, was
implicated to carry out selections in Brassica and wheat (Ristic
et al. 2007, Kumar et al. 2013). Further, higher pollen grain fer-
tility under HS may serve as an important criterion for measur-
ing HT (Rodriguez-Garay and Barrow 1988). Targeting pollen
selection under HS in cotton, heat-tolerant genes were transferred
from a donor line 7456 (G. barbadense L.) to a heat-sensitive
genotype Paymaster 404 through backcrossing (Rodriguez-
Garay and Barrow 1988). In addition to pollen selection, relative
cell injury level (RCIL) under HS could also be taken as a
reliable index in determining HS tolerance in cotton (Sullivan
1972, Khan et al. 2008). Similarly, Petolino et al. (1992) pro-
posed gametic selection as a viable option for addressing HS in
maize.
With regard to root traits, adaptation of root respiratory carbon
metabolism can offer tolerance to soil temperature by managing
the ion uptake load as investigated in Agrostis species (Rachmi-
levitch et al. 2006). Furthermore, Huang et al. (2012) deduced
that the efficient carbon and protein metabolism conferred higher
thermotolerance to roots at 45C in Agrostis scabra (a C3 peren-
nial grass species). From phenology point of view, selection of
early flowering and maturity could enable us to escape HS in
spring-sown chickpea in Mediterranean region and south India
(Toker et al. 2007, Berger et al. 2011). Likewise, early-maturity-
led escape mechanism enabled addressing HS in wheat in East-
ern Gangetic Plains and various South Asian locations (Joshi
et al. 2007a, Mondal et al. 2013). Stay green or delayed senes-
cence imparts yield improvement under abiotic stress (Thomas
and Smart 1993, Borrell et al. 2000, Thomas and Howarth 2000,
Harris et al. 2007). Screening of a total of 963 diverse wheat
accessions at various sowing time suggested that stay-green trait
associated with CTD could be a strong indicator of HT (Kumari
et al. 2007). However, stay-green trait is less important in the con-
text of yield on account of disability in translocation of stem
reserves to grain under HS (Blum 1998). While under conditions
encompassing HS alone as well as HS and drought, stay-green trait
measured as normalized difference vegetation index (NDVI) at
physiological maturity exhibited a positive correlation with yield
6 U. C. JHA, A. BOHRA,
(Lopes and Reynolds 2012). Therefore, physiological trait-based
breeding remains a promising improvement strategy to develop
heat-tolerant genotypes without causing yield penalty.
Intervention of Molecular Markers for HT Breeding
QTL identification and trait mapping by molecular markers
To date, conventional breeding schemes have been extensively
deployed for uncovering the HT-relevant gene(s) and their
inheritance patterns, thus illuminating the causal molecular
mechanism (Wahid et al. 2007, Farooq et al. 2011). To this
end, advances in DNA marker discovery and genotyping
assays have permitted the accurate determination of chromo-
somal position of the QTLs responsible for HT in different
crops (Jagadish et al. 2010a, Pinto et al. 2010, Paliwal et al.
2012, Bonneau et al. 2013). An updated list of QTLs associ-
ated with HT in various crops is shown in Table 1. Further,
information related to important QTLs controlling tolerance
against various abiotic stresses in different crops can be
accessed from PLANTSTRESS site (http://www.plantstress.
com/biotech/index.asp?Flag=1).
By applying 245 restriction fragment length polymorphism
(RFLP) markers in 98 backcross inbred lines (BILs) derived
from the cross (Nipponbare 9 Kasalath) 9 Nipponbare, three
QTLs for HT were detected each on chromosome 1, 4 and 7
(Zhu et al. 2005). These three QTLs explained 8.94%, 17.25%
and 13.50%, respectively, of the entire PV during grain-filling
stage (Zhu et al. 2005). In addition to QTL analysis, application
of BSA using a set of SSR markers in 279 F2 (996 9 4628)
individuals resulted in identification of two loci associated with
HT, viz. RM3735 (chromosome 4) and RM3586 (chromosome
3), that controlled 17% and 3% proportions, respectively, of the
total PV (Gui-lian et al. 2009). Similarly, eight QTLs governing
spike fertility under high temperature were mapped on different
chromosomes, such as 1, 2, 3, 8, 10 and 11 (Jagadish et al.
2010a). Recently, a major dominant locus OsHTAS (Oryza sativa
heat tolerance at seedling stage) was identified from the geno-
type HT54, which contributed high temperature tolerance at
48C especially during seedling and grain-filling stages (Wei
et al. 2013). Likewise, two major QTLs for HT, namely
qHTSF1.1 (R2 = 12.6%) and qHTSF4.1 (R2 = 17.6%), were
detected on chromosome 1 and 4, respectively, in BC1F1 and F2
progeny generated from the cross IR64 9 N22 (Ye et al. 2012).
Recently, a QTL study involving 90 introgression lines provided
five QTLs explaining PVs in the range of 6.8314.63% (Lei
et al. 2013). An introgression line Y106 carrying two QTLs for
HS tolerance (qHTS1-1 and qHTS3) was identified while trans-
ferring genes from the wild rice (O. rufipogon Griff.) (Lei et al.
2013).
Under terminal HS, various physiological and agronomic traits
contributing to grain yield improvement or yield components
directly or indirectly in wheat have been discussed using multi-
environment analysis (Mason et al. 2011, Bennett et al. 2012,
Paliwal et al. 2012, Bonneau et al. 2013). In wheat, evaluation
of senescence-related traits revealed nine QTLs across different
chromosomes (2A, 6A, 6B, 3A, 3B and 7A) (Vijayalakshmi
et al. 2010). A heat susceptibility index (HSI) was constructed
using parameters such as spike yield and temperature depression
(TD) of spike, and subsequently, a total of 14 QTLs associated
with HSI were discovered (Mason et al. 2011). Following
sodium dodecyl sulphate sedimentation (SDSS) test, four QTLs
for improved baking quality under HS conditions were found on
wheat chromosomes 1B, 1D, 4A and 7A (Beecher et al. 2012).
AND N. P. SINGH
Three major QTLs associated with HT were mapped on
chromosomes 2B, 7B and 7D in 148 RILs (NW1014 9 HUW468),
accounting up to 20% PV (Paliwal et al. 2012).
Considering grain-filling rate (GFR) as a pivotal trait govern-
ing grain yield in wheat, BSA was employed using SSR markers
in an F2 population of Ksu106 9 Yecora Rojo (Barakat et al.
2012). As a result, 12 SSR markers were found to be in close
association with GFR in wheat. Similarly, Kirigwi et al. (2007)
mapped QTLs for GFR on 4A chromosome. Under HS, a major
QTL experiencing 17% variation on yield was detected on chro-
mosome 4A in wheat (Pinto et al. 2010). Given amenability of
single nucleotide polymorphism (SNP) markers to automated
genotyping assays, one candidate SNP marker was discovered
recently in wheat that markedly distinguished heat-tolerant
(K7903) and heat-sensitive (RAJ4014) cultivars (Garg et al.
2012). More recently, genome-wide as well as candidate-gene-
based association mapping approaches using SNP and diversity
array technology (DArT) were applied in chickpea to establish
markertrait associations for HT (Thudi et al. 2014).
Importantly, most desirable yield-relevant physiological traits
and their respective chromosomal locations are discussed in
wheat (Cossani and Reynolds 2012). In case of maize, 184
RFLP markers were employed in a RIL population, which led to
the detection of five QTLs controlling pollen germination, and
six QTLs for pollen tube growth under HS (Frova and Sari-Gor-
la 1994). Earlier, using the same mapping population, six QTLs
were identified in maize that controlled cellular membrane stabil-
ity under HS (Ottaviano et al. 1991). In sorghum, four QTLs
(Stg14) related to stay green trait were mapped on three LGs,
viz. A, D and J. Importantly, co-occurrence of QTLs, namely
Stg1 and Stg2, with important photosynthetic genes and HSPs
on LG A strongly supported the involvement of LG A in
response to heat and drought stress (Xu et al. 2000). In case of
adzuki bean, two QTLs, viz.HQTL1 and HQTL2, were identified
for enhancing pollen viability under HS (Kaga et al. 2003,
Vaughan et al. 2005). Similarly, applying SNP marker in a RIL
population (CB27 9 IT82E-18), Lucas et al. (2013) reported
five important genomic regions that rendered HT in cowpea. In
tomato, six QTLs were found to be linked with fruit set under
HS (Grilli et al. 2007). Additionally, Xiang-yang et al. (2008)
identified two QTLs conferring HT in tomato. Deploying ampli-
fied fragment length polymorphism (AFLP) and random
amplified polymorphic DNA (RAPD) markers aided in the iden-
tification of five QTLs related to HT in Brassica campestris L.
ssp. pekinensis (Shuancang et al. 2003). The above-mentioned
QTLs identified using molecular markers in different crops pro-
vide a way to transfer the causative heat-tolerant gene(s)/QTLs
to elite cultivars. In parallel, the fine mapping accompanied by
cloning of candidate QTL will help the breeders to commence
marker-assisted breeding for incorporating HT in various impor-
tant crops in near future.
Markers assisted introgression of HT-relevant traits: A faster
breeding strategy
Molecular markers enabling recovery of desirable genotypes in a
precise and time-saving fashion become imperative while deal-
ing with quantitative traits such as HT (Shirasawa et al. 2013).
In rice, a marker-based approach, that is, advanced backcross,
was used to develop introgression lines in the background of
Teqing, and later, screening of these lines allowed detection of
one heat-sensitive line YIL106 (Lei et al. 2013). Similarly,
heat-tolerant (XN0437T) and heat-sensitive (XN0437S) intro-
Table 1: List of QTLs/gene(s) conditioning HT in different crops

Markers linked Chromosomal location/

Crop to the QTLs Name/No. of the QTL/loci Linkage group (LG) Mapping population Range of PV (%) References

Arabidopsis SNP 5 THERM QTLS (THERM1e, THERM3.e, THER4.1.e, 1, 3, 4, 4 and 5 - 7 Li et al. (2014a,b),
THERM4.2.e and THERM5.e)
Azuki bean - HQTL1 and HQTL2 pollen viability under HS BC (Vigna riukiuensis 9 V. angularis) - Kaga et al. (2003),
Vaughan et al. (2005),
Heat stress in crop plants

Tomooka et al. (2011),

Barley SSR 34 putative QTLs - BC2DH (Scarlett 9 ISR42-8) - Mohammed (2004)
Brassica AFLP, RAPD 5 QTLs Three different LG - Shuancang et al. (2003)
Cowpea SNP Five regions of 9% of the cowpea genome, Cht-3 RIL (CB27 IT 9 82E-18) 11.518.1 Lucas et al. (2013)
SNP Hbs1, Hbs2 and Hbs3 IT93K-503-1 9 CB46 6.277.3 Pottorff et al. (2014)
IT84S-2246 9 TVu14676
Maize RFLP 6 QTLs (cellular membrane stability) RIL (T232 9 CM37) - Ottaviano et al. (1991)
RFLP 38 QTLs, heat-shock protein (HSP) expression - RIL (T232 9 CM37) - Frova and Sari-Gorla
(1993),
RFLP 5 QTLs for IPGG and six QTLs for IPTG. - RIL (T232 9 CM37) - Frova and Sari-Gorla (1994)
Potato AFLP, SSR QTLs resistance to internal heat necrosis (IHN) LG 4, 5, 7 and 10 RIL (Atlantic 9 B1829-5) - McCord et al. (2011)
Rice - qhr1, qhr3-1, qhr4-3, qhr8-1, qhr11-1 and qhr11-2 1, 3, 4, 8 and 11 DH (IR64 9 Azucena) 1.322.8 Cao et al. (2003)
RFLP 3 QTLs 1, 4 and 7 BIL Nipponbare/Kasalath//Nipponbare 8.9417.25 Zhu et al. (2005)
- 9 QTLs thermotolerance for amylose content and gel 6 and 8 Nipponbare/Kasalath//Nipponbare - Zhu et al. (2006a)
consistency
SSR WBKqWK1-1, qWK1-2, qWK2 and qWK8 1, 2 and 8 RIL (Chiyonishiki 9 Koshijiwase) 8.815 Tabata et al. (2007)
SSR 2 putative QTLs associated with white-back kernels 4, 6 (Hana-echizen 9 Niigata-wase) 15.259.6 Kobayashi et al. (2007)
SSR qHt3, qHt9a 3 and 9 RIL (T219 9 T226) 7.611.4 Chen et al. (2008)
SSR 3 QTLs (qhts-2, qhts-3 and qhts-5) LG 2, 3 and 5 RIL (Zhongyouzao No. 8 9 Fengjin) 6.5910.72 Zhang et al. (2008)
SSR RM3735 and RM3586 loci 4 and 3 F2 (996 9 4628) 317 Gui-lian et al. (2009)
- qtl_2.3,qtl_4.1, qtl_1.1,qtl_2.2,qtl_8.2,qtl_1.1,qtl_8.1, 1, 2, 3, 4, 8, 10, 11 (Bala 9 Azucena) 717.6 Jagadish et al. (2010a)
qtl_10.1,qtl_1.1,qtl_3.4,qtl_8.3,qtl_10.1,
qtl_1.1,qtl_11.1,qtl_10.1,qtl_1.1,qtl_10.1 and qtl_11.1
SSR 2 QTLs 4 and 10 RIL (996 9 4628) 21.325.8 Xiao et al. (2011)
11.511.6
SSR qPF4, qPF6 4 and 6 RIL (996 9 4628) 15.19.31 Ying-hui et al. (2011)
SNP qHTSF1.1 1 BC1F1, BC2F2 and F2 (IR64 9 N22) 12.617.6 Ye et al. (2012)
qHTSF4.1 4
SNP OsHTAS locus 9 F1 and F2 (HT54 9 HT13) - Wei et al. (2013)
SSR qHTS1-1 1 Introgressed line YIL106 6.8314.63 Lei et al. (2013)
SSR qHTS1-2, qHTS2, qHTS3 and qHTS8 1, 2, 3 and 8 (Teqing 9 O. rufipogon)
SSR (qWB3, qWB4, qWB6 and qWB9) QTLs for WBK 3, 4, 6 and 9 for WBK (Hana-echizen 9 Niigata-wase) (31.536.8) WBK Kobayashi et al. (2013)
(qKW3-1, qKW3-2, qKW6, qKW7 and KW10) QTLs 3, 3, 6, 7 and 10 (8.412.1) DTH
for KW for KW
(qDH1, qDH3 and qDH6) QTLs for DTH 1, 3 and 6 for DTH
SSR SNP QTL for white-back grains 6 RIL (Tohoku 168 9 Kokoromachi) - Shirasawa et al. (2013)
SSR 9 QTLs 3, 4, 6, 8, 10 and 11 BC2F2 (OM5930x N22) 17.136.2 Buu et al. (2014)
Sorghum RFLP Stg 1, Stg 2, Stg 3 LGA, LGD and LGJ RIL 46 Xu et al. (2000)
Stg 1, Stg 2 responsible for heat-shock protein
expression

(continued)
7
 8
Table 1: (continued)

Markers linked Chromosomal location/

Crop to the QTLs Name/No. of the QTL/loci Linkage group (LG) Mapping population Range of PV (%) References

Tomato fAFLP QTLs related to fruit set under HS 1, 3, 4, 6, 7 and 9 F2 (Jab-95 9 Caribe) 32.8 Grilli et al. (2007)
RAPD and SSR 2 QTLs LG3 and LG7 F2 (01137 9 CLN2001A) - Xiang-yang et al. (2008)
- 29 putative QTLs, 2 QTLs contributed in viability of RIL (CLN1621 L 9 CA4) - Schafleitner (2014)
pollen under HS
Wheat SSR 1.4 genes (Ventnor 9 Karl 92) - Yang et al. (2002)
SSR 2 QTLs (Ventnor 9 Karl92) 1112. Yang et al. (2002)
AFLP and SSR 3 QTLs LG1B, 5B and 7B RIL (Kauz 9 MTRWA116) 27.344.3 Mohammadi et al. (2008)
SSR Common QTL for drought and heat stress traits 1B-a, 2B-a, 3B-b, 4A-a, RIL (Seri 9 Babax) 17 (yield QTL) Pinto et al. (2010)
4B-b, and 7A-a 28 (CT)
AFLP, SSR (Q75%Gh.ksu-2A, Q75%Gh.ksu-2A, 2A, 6B, 3A, and 7A RILs (Ventnor 9 Karl 92) 53 (75%Q), Vijayalakshmi et al. (2010)
Q75%Gh.ksu- 3B) 75%G, 28 (25%G),
(Q25%Gh.ksu-2A, Q25%Gh.ksu-2A) 25%G, 63 (50%G),
(Q50%Gh.ksu-2A, Q50%Gh.ksu-6A) 50%G, 40 (MRS),
(QMrsh.ksu-2A)
(QTmrsh.ksu-2A, QTmrsh.ksu-6A, QTmrsh.ksu-6B) 55 (TMRS),
TMRS,
(QPgmsh.ksu-3A, QPgmsh.ksu-6B) PGMS, 36.4 (PGMS),
(QFv/Fmh.ksu-7A) Fv/Fm 11.2 (Fv/Fm)
SSR 5 QTLs 1A, 2A, 2B, and 3B RIL (Halberd 9 Cutter) Mason et al. (2010)
associated with HIS
SSR 3 QTLs (QSg. bhu-1A, QSg.bhu-3B and QSg.bhu-7D) 1AS, 3BS and 7DS RIL (Chirya3 x Sonalika) 38.7 Kumar et al. (2010)
SSR 14 QTLs for heat susceptibility index (HIS) 1B, 3B, 4A, 5A, F2:6 RIL (Halberd 9 Karl 92) Individual QTL Mason et al. (2011)
7 QTLs colocalized for HIS and TD trait 5B and 6D (4.519.3)
SSR Xgwm132-linked QTL, Xgwm577-linked QTL and 6B, 7B and 6A F1, F2 (Debra 9 Yecora Rojo) 325. Barakat et al. (2011)
Xgwm617-
linked QTL
SSR 12 QTLs 1A, 7A, (3B, 3A, 5B), F2 (Ksu106 9 Yecora Rojo) 2264 Barakat et al. (2012)
2D, 1D, (2A, 2B,
2D),
SSR QHthsitgw.bhu-2B, QHthsitgw.bhu-7B, QHthsitgw.bhu- 1B, 7D, (4A, 5D), RIL (NW1014 9 HUW468) 9.78-20.34 (TGW) Paliwal et al. (2012)
7D, (TGW), QHthsiYLD.bhu-7B, QlsYLD.bhu-7B, (7A, 7B, 7D), 5A 13.21 (YLD),
(YLD), QHthsigfd.bhu-2B (GFD), QHtctd.bhu-7B and 3B, BL, 7BL, 20.15 (GFD),
(CTD), Qls- 7DS (TGW), 7BL 19.81 (CTD) and
dm.bhu-7D (DM) (YLD) 7.42 (DM)
2B1 (GFD), 7BL
(CTD) and 7DS
(DM)
DArT and SSR 2 QTLs, (Q.Yld.aww-3B-2 and Q.Yld.aww-3D) 3B DH, RIL (RAC875 9 Kukri) 22 Bennett et al. (2012)
SSR 4 QTLs (Qsdscon.tam-1B, Qsdsheat.tam-1D, LG 1B, 1D, 4A, RILs (Halberd 9 Cutter) 1830 Beecher et al. (2012)
Qsdscon.tam-4A and Qsdssta.tam-7A) and 7A
SSR Marker locus gwm299 3BL DH, RIL (RAC875 9 Kukri) - Bonneau et al. (2013)
U. C. JHA, A. BOHRA,

AFLP, SSR, DArT TKW QTLs linked or pleiotropic to DH and DM 4B and 7D-b RIL (Barbax 9 Seri) 39 (TKW) Lopes et al. (2013)
AFLP, SSR, DArT Few QTLs associated with ECG 7D-a and 7D-b RIL (Barbax 9 Seri) 17.4 (ECG) Lopes et al. (2013)
AND

AFLP, SSR, DArT Consistent QTLs were detected for CTvg and CTgf 4A RIL (Barbax 9 Seri) 16 (Ctgf) Lopes et al. (2013)

(continued)
N. P. SINGH
Heat stress in crop plants 9

BC, backcross; BILs, Backcross inbred lines; TKW, thousand-kernel wt; DH, Double Haploid; DM, days to maturity; HS, heat stress; HSI, Heat susceptibility index; GY, Grain yield; TGW, Thousand grain
weight; GFD, Grain-Filling duration; CT, Canopy temperature; TD, Temperature depression; CTD, canopy temperature depression; PV, phenotypic variation; IPGG, pollen germinability; IPTG, pollen tube
gression lines were also recovered from another backcross

growth; WBK, white-back kernels; KW, 1000 kernel weight; DTH, days to heading; EGC, Early ground cover; CTvg, Canopy temperature under vegetative growth; CTgf, Canopy temperature under grain-filling
stage; 75%G, 75% green; 25%G, 25% green; 50%G, 50% green; MRS, maximum rate of senescence; TMRS, time to maximum rate of senescence; PGMS, percentage greenness at maximum senescence; Fv/Fm,
inbred population derived from the cross (Xieqingzao
B 9 N22) 9 Xieqingzao B (Jiang-lin et al. 2011). Near-

Mondal et al. (2014)

Tiwari et al. (2013)
isogenic lines (NILs) created by introducing qWB6-allele from
Ali et al. (2013)
Hana-echizen into the background of Niigata-wase showed
References

considerable reduction in the incidence of heat-induced injuries

such as white-back kernels (Kobayashi et al. 2013). In a recent
study conducted in rice, a 1.5-Mb chromosomal region delimited
with markers ktIndel001 and RFT1 was transferred from Kok-
oromachi to Tohoku 168 using marker-assisted backcrossing.
Range of PV (%)

And the resultant NILs had grain quality significantly improved

over the susceptible parent Tohoku 168. The genomic region
involved above actually harboured a robust QTL that controlled
812

better grain quality under HS, and governed more than 20% of
the entire PV (Shirasawa et al. 2013). A non-exhaustive list of
-
-

DNA markers related to various HT/component traits available

in different crops is presented in Table 2. With such robust
markers/candidate gene(s)/QTLs in place, marker-based selection
in early generations accompanied by a strategic mating scheme
19 families consisting of 384
individuals developed from

would maximize the genetic gains while breeding for HT.

DH (Berkut 9 Krichauff)

RIL (Halberd 9 Karl 92)

Mapping population

Progress in Proteomics and Functional Genomics:

Expression Profiles and Candidate Genes for HT
3-way cross

Emerging trends in functional genomics facilitate elucidation of

the role of candidate genes, genome-wide expression analysis
and HS response coupled with regulatory and tolerance mecha-
nism for HS in plant (Sreenivasulu et al. 2007, Vij and Tyagi
Chromosomal location/

2007, Urano et al. 2010).

Linkage group (LG)

1D, 6B, 2D and 7A

Following proteomics analysis, a total of 54 proteins involved

in carbohydrate metabolism, protein synthesis and stress
responses during caryopsis were identified in rice under HS con-
1B and 5A

dition (Lin et al. 2005). By conducting a similar proteomic

study, thermotolerance was noticed in the roots of Agrostis sca-
bra (heat tolerant) at different temperature levels, and the study
-

indicated an up-regulation of proteins in comparison with sensi-

tive species of A. stolonifera (Xu and Huang 2009). Likewise,
7 QTLs associated with HSI traits, GFD, TGW, GY
QChlc.tamu-1B (chlorophyll content), QFlt.tamu-2B

QTL for leaf and spike temperature depression and

new insights were gained related to HSPs and regulatory pro-

9 QTLs associated with GFD, TGW, GY and CT

teins, energy metabolism and redox homeostasis by applying

MALDI-TOF MS in rice (Lee et al. 2007). Leaf proteome analy-
sis of wild rice O. meridionalis (under HS at 45C) manifested
differential response of heat-responsive genes and encouraged
enzymes associated with Calvin cycle and thiamine biosynthesis
(FLTD), QIkw.tamu-5A (IKW)

(Scafaro et al. 2010). Thirteen differentially expressed protein

Name/No. of the QTL/loci

spots identified by MASS/MALDI-TOF analysis under HS dur-

ing anthesis shed new light on the mechanism of HT in rice
(Jagadish et al. 2010b). Further, differential expressions of phos-
phoproteins under HS were also examined in rice leaves (Chen
et al. 2011). Similarly in maize, MALDI-TOF mass spectrometry
under HS

leaf wax

allowed detection of sHSP17.4, sHSP17.2 and sHSP26 proteins

and CT

under combined drought and HS (Hu et al. 2010). MALDI-TOF/

TOF analysis also facilitated identification of 81 differentially
expressed proteins in alfalfa, thereby furnishing new clues about
the molecular basis of HS response (Li et al. 2013a). By apply-
Markers linked

ing novel proteomic approach, that is, multidimensional protein

to the QTLs

identification technology (MudPIT), the role of stomatal proteins

chlorophyll fluorescence.

was examined and consequently, up-regulation and down-regula-

Table 1: (continued)

SSR

SSR

tion of genes under HS condition in Agave americana was

experimentally demonstrated (Shakeel et al. 2013). High levels
of six leaf proteins and nine root proteins were obtained in trans-
genic A. stolonifera, harbouring isopentenyl transferase (ipt) gene
that manages HT via regulating cytokinin synthesis (Xu et al.
Crop

2010).
10 U. C. JHA, A. BOHRA, AND N. P. SINGH

Table 2: Robust DNA markers to enable faster breeding for HT in various crops

Crop Trait Marker References

Cowpea Pod set 1_1346, 1_0437 (SNP) Lucas et al. (2013)

Seed coat 1_0032, 1_1128 and 1_0640 (SNP) Pottorff et al. (2014)
Rice Seedling stage HT InDel5 and RM7364 Wei et al. (2013)
Flowering stage and spikelet fertility SNP17877584, SNP19381891 (SNP); RM570- Ye et al. (2012), Chen et al. (2008),
RM148 (SSR), B1065E10 Jagadish et al. (2010a)
Seed set percentage M5687 and RM471, RM6132-RM6100 (SSR) Xiao et al. (2011), Ye et al. (2012)
Filled grains per panicle and grain yield RM3586, RM3735 and RM160 (SSR) Zhang et al. (2009b), Gui-lian et al. (2009),
Buu et al. (2014)
Days to heading RM151, RM5172 and RM1369 (SSR) Kobayashi et al. (2013)
Kernel weight RM7365 (SSR) Kobayashi et al. (2013)
White-back kernel RM3288 and RM8125 (SSR) Kobayashi et al. (2007), Kobayashi et al.
(2013)
Yield RM5749 and RM337 (SSR) Buu et al. (2014)
Tomato Fruit set fAFLP Grilli et al. (2007)
Wheat Grain-filling duration (GFD) Gwm293, gwm11, Xcfd43 (SSR) Yang et al. (2002), Mohammadi et al. (2008),
Sadat et al. (2013)
Grain-filling duration Xwmc 407, Xbarc137 (SSR) Mason et al. (2010, 2011), Sadat et al. (2013)
Grain-filling rate Xgwm 577 Barakat et al. (2011), Paliwal et al. (2012)
Kernel weight gwm291, Gwm268, WMC527 (SSR) Mason et al. (2010, 2011), Sadat et al. (2013)
CTv wPt-3465, agg/cta-12, acc/ctc-8, aag/cta-7 Pinto et al. (2010)
CTg gwm388 (SSR) Pinto et al. (2010)
GM barc065, act/cag-5, wPt-0021 Pinto et al. (2010)
TGW aag/cta-5 Pinto et al. (2010)
75%G, 25%G Xgwm356/CGT.TGCG-349 Vijayalakshmi et al. (2010)
MRS CAG.AGC-101/AGG.CTT-212 (AFLP) Vijayalakshmi et al. (2010)
PGMS Xbarc198/CGT.CTCG-406 Vijayalakshmi et al. (2010)
TMRS Xgwm111/Xgwm437 (SSR); Xgwm356/ Vijayalakshmi et al. (2010)
CGT.TGCG-349
HSITGW, HSIGFD and CTD Xgwm1025Xgwm745, Xgwm935 Paliwal et al. (2012)
Xgwm1273, Xgwm1025Xgwm745 (SSR)
Canopy temperature, early vigour, RAC875 allele Bennett et al. (2012)
flag leaf width, peduncle length
Baking quality barc170, wmc468, wmc707, barc119, Beecher et al. (2012)
gwm337 (SSR)
Yield act/cag-5, gwm397 Pinto et al. (2010)
Grain yield and thousand-grain weight gwm299 (SSR) Bonneau et al. (2013)

G, green; CTv, canopy temperature in the vegetative stage; CTg, canopy temperature in the grain-filling stage; TGW, thousand grain weight; GM,
grain number; MRS, maximum rate of senescence; PGMS, percentage greenness at maximum senescence; TMRS, time to maximum rate of senes-
cence.

Relating to gene expression profiling under high temperature,
22-K DNA microarray, differential hybridization and reverse
transcription-PCR were undertaken to examine the regulation of
different starch synthesis genes, viz. granule-bound starch syn-
thase I (GBSSI) and branching enzymes (BEIIb) associated with
grain filling in rice (Yamakawa et al. 2007). Microarray-based
expression analysis of rice pollens that were exposed to high
temperature revealed down-regulation of some important tape-
tum-specific genes under HS, however other genes like Osc6,
OsRAFTIN and TDR genes remained unaffected during high
temperature (Endo et al. 2009). In addition, by combining micro-
array and cDNA-AFLP techniques, Bita et al. (2011) demon-
strated the transcriptomic response of meiotic anthers in heat-
tolerant as well as in heat-sensitive tomato genotypes. As a
result, this study provided a set of candidate genes conferring
HS tolerance in tomato.
Transcriptome analysis using Affymetrix Grape genome oligo-
nucleotide microarray elucidated stress-responsive genes, and the
transcription factors involved in HS. Moreover, the role of HSPs,
ascorbate peroxidase and galactinol synthase in imparting HT
was also elucidated (Liu et al. 2012). Similarly, application of
Affymetrix 22K Barley 1 Gene Chip microarray illustrated the
expression patterns of 958 induced genes and 1122 repressed
genes during caryopsis development in barley observed under
early HS (Mangelsen et al. 2011). Further, this investigation also
indicated that the embryo and endosperm are the prime locations
for HS response (Mangelsen et al. 2011). Involvement of differ-
ent HSPs with reactive oxygen species (ROS), hormones and
sugars was tested in tomato by affymetrix tomato genome array
and cDNA-AFLP-based transcriptome profiling (Frank et al.
2009). Likewise, genome-wide expression patterns of genes were
analysed in sensitive and tolerant wheat lines using GeneChip
wheat genome array, thereby enabling access to the HS-respon-
sive genes (Qin et al. 2008). A similar transcriptome analysis in
potato under high soil temperature uncovered a suite of stress-
related genes that encode for HSPs in periderm (Ginzberg et al.
2011).
A comprehensive genome-wide translational analysis clearly
depicted a decrease in translation process under HS in Arabidop-
sis (Y
anguez et al. 2013). Given the role of non-coding RNAs
in abiotic stress tolerance (Chinnusamy et al. 2007), response of
chloroplast small RNA (csRNA) under HS and their prospects in
engineering HT in Chinese cabbage were discussed (Wang et al.
2011). Recently, deep sequencing of RNA produced a novel
class of conserved RNA and miRNA concerned to heat response
in B. rapa, notably the bra-miR398a and bra-miR398b (heat
inhibitive) and bra-miR156 h and bra-miR156 g (Yu et al.
2012). Similarly, several heat-responsive miRNA and genes were
identified in various plants by applying transcriptome sequencing
(Table 3). More recently, a comparative transcriptomic analysis
Table 3: Application of deep transcriptome sequencing for identification of heat-responsive gene(s) and regulatory RNA molecules in various plant species
Crop
Apium graveolens L.
Arabidopsis thaliana
Arabidopsis thaliana
Brachypodium distachyon
Brassica rapa ssp. Chinensis
Brassica rapa
B. rapa ssp. pekinensis and
B. rapa ssp. chinensis
Cicer arietinum
Gossypium hirsutum L.
G. barbadense L.
Menihot esculenta Crantz
Oryza sativa
Populus tomentosa
Panex. ginseng C.A. Meyer
Rhazya stricta
Solanum lycopersicum
Triticum aestivum L.
Triticum aestivum L.
Triticum aestivum L.
Triticum aestivum L.
Youngia japonica
csRNA, Chloroplast small RNA; npcRNAs, non-protein-coding RNA.
Heat stress in crop plants
Tissue used for cDNA
Genotype library construction Platform used Candidate genes/regulatory RNA Reference
Ventura and Jinnan Shiqin Leave Illumina HiSeq 2000 celery-89505, celery-28253, celery-20717 Li et al. (2014a)
and celery-18591
celery-10247 and celery-75186 genes
- Leave Solexa sRNA-encoding genes Baev et al. (2013)
- - Illumina GAIIx sequencer SR45a mRNA Gulledge et al. (2012)
- Diverse array of tissue Illumina 1088 heat-responsive genes Priest et al. (2014)
Wu11 Seedlings Illumina Genome Analyzer Heat-responsive csRNA Wang et al. (2011)
Wu11 Above ground part of Illumina GAII sequencer BracCSD1 and BracSPL2 genes Yu et al. (2012)
seedling
Bre and Wut Seedlings Illumina GAII 728 novel cis-natural antisense transcripts Yu et al. (2013)
(cis-NATs)
Heat cis-NATs-derived small interfering
RNAs
ICC4958 Embryo, leaves, apical Illuminas Genome Analyzer I DNAJ heat-shock protein Hiremath et al. (2011)
meristem, shoots, roots, Heat-shock proteins (HSP 70, HSP 91)
buds, flowers and pods
Guazuncho 2 Fibres 454 GSFLXTM Titanium 28 heat-shock protein-annotated genes Lacape et al. (2012)
VH8-4602
TAI16 Root and leave Illumina Genome analyser 134 target genes for conserved miRNA Ball
en-Taborda et al. (2013)
sequence and 1002 genes for non-
conserved miRNA
- Shoot and root Illumina 39 known miRNAs and 173 miRNAs Mangrauthia et al. (2013)
- Solexa sequencing 52 miRNAs Chen et al. (2012b)
Shizhu Leaf, stem, flower and root Illumina sequencing 10 heat-responsive miRNA Wu et al. (2012)
- Leave Illumina HiSeq 2000 - Yates et al. (2014)
- Root Illumina GAIIX 3 class I heat-shock protein genes Gupta et al. (2013)
Chinese spring and TAM 107 Leave Solexa TaGAMYB1 and TaGAMYB2 Xin et al. (2010)
Chinese spring and TAM 107 Seed Solexa Long npcRNAs (TahlnRNA12, TahlnRNA23 Xin et al. (2011)
and TahlnRNA29)
PBW343 Seed Illumina GAIIx tae_7, tae_10, tae_15, tae_19, tae_22, tae_45 Pandey et al. (2014)
HD2985 and NIAW Seed Illumina Hiseq 2000 HSF3, HSFA4a, HSP17, HSP70 and Goswami et al. (2014)
superoxide dismutase (SOD)
- Leave Illumina Genome Analyzer T1 Unigene BMK.37824 Peng et al. (2014)
11
12 U. C. JHA, A. BOHRA, AND N. P. SINGH

Germplasm Resources
Physiological adaptive/morphological traits Cultivars/landraces, Crop wild relatives,
Core/minicore collection, Experimental populations

genomic libraries
Molecular

BAC and other

Sanger/ NGS
markers

Modern Molecular Tools

cDNA library
Precise Molecular maps
High throughput
Phenomics

Screening
phenotyping

ESTs
Candidate Gene/QTL
discovery

Unigenes

RNA
Improved

Seq
Introgression into different
cultivars genetic backgrounds

expression profile
Field and multi

Genome wide

Regulatory RNA
location/multiyear

Tentative unique
Transcriptome

Microarrays
trials

sequences
HS Tolerant assembly
Cultivar Fig. 1: An integrated breeding
NGS=Next Generation Sequencing
BAC=Bacterial artificial chromosome strategy for improving heat
tolerance in crops

investigated the role of 16 common genes in protein refolding Jiang et al. 2009, Khurana et al. 2013, Li et al. 2013c, Zhang
process in switchgrass, rice, wheat and maize (Li et al. 2013b). et al. 2013) and tobacco (Sanmiya et al. 2004, Sun et al. 2012).
Genome-wide transcriptional response of 10 ecotypes of The regulatory role of DREB gene family [a class of Apetala 2
Arabidopsis thaliana under HS was investigated by employing (AP2) transcription factor] in generating abiotic stress response
Arabidopsis Nimble Gen ATH6 microarrays (Barah et al. 2013). in various crops under stressed conditions has been thoroughly
Further, in silico transcript regulatory network model in Arabid- reviewed (Sakuma et al. 2006, Qin et al. 2007, Shinozaki and
opsis presented 35 TFs showing ecotype-specific response to HS Yamaguchi-Shinozaki 2007, Lata and Prasad 2011). Higher
(Barah et al. 2013). Taken the above description into account, it expression of OsDREB2B gene in rice (Matsukura et al. 2010)
is expected that the proteomics and functional genomics can and greater response of ZmDREB2A gene in maize (Qin et al.
greatly expedite the progress of discovery and functional charac- 2007) may cause induction of heat-responsive genes providing
terization of the heat-tolerant genes/QTLs. A comprehensive adaptation and survival under HS. Similarly, Mizoi et al. (2013)
approach involving multiple disciplines to combat HS is given have reported activation of GmDREB2A in soybean under HS.
in Fig. 1. This gene family is known to be associated with HT in various
plant species such as chrysanthemum (Hong et al. 2009) and
Arabidopsis (Lim et al. 2007, Qin et al. 2007, Matsukura et al.
Genetic Manipulation of HT Using Transgenic 2010). Likewise, expression of CAP2 gene (another class of
Technologies AP2 transcription factor) caused high germination efficiency in
With increasingly refined transformation and regeneration proto- transgenic tobacco under HS (Shukla et al. 2009). Genetic engi-
cols, transgenic techniques are becoming attractive tool for neering of membrane lipid causing increase in accumulation of
designing both biotic and abiotic stress-tolerant crops via manip- saturated fatty acid offers high temperature tolerance in plants
ulating native genes or introducing gene (s) that lie beyond the (Grover et al. 2013). This property has been well exploited by
crop gene pools (Ashraf et al. 2008). In the context of HT, silencing chloroplast omega-3 fatty acid desaturase gene, which
genetic engineering has focused so far primarily on engineering led to lowering in trienoic fatty acids in tobacco, thereby impart-
genes that encode TFs, HSPs, chaperones, organic osmolytes, ing adaptation to high temperature (Murakami et al. 2000). The
antioxidants and plant growth regulators (Ashraf 2010, Grover omega-3 fatty acid desaturase gene was also found to be
et al. 2013). The detailed list of important transgenes contribut- involved in high temperature tolerance in transgenic tomato,
ing to various abiotic stresses including HT is provided in which had reduced activity of endoplasmic reticulum (Wang
PLANTSTRESS site (http://www.plantstress.com/biotech/index. et al. 2010).
asp?Flag=1). Concerning osmolyte compounds that contribute to HS toler-
Recently, Grover et al. (2013) reviewed genetic manipulation ance, transformation of Arabidopsis harbouring cod gene from
of HSF and HSP genes and the related change in expression lev- Arthrobacter globiformis resulted in substantial accumulation of
els under HS. Over-expression of HSFs is successfully demon- glycinebetaine, leading to acclimation against high temperature
strated in tomato (Mishra et al. 2002, Giorno et al. 2010), (Alia et al. 1998). Biosynthesis of glycinebetaine offers high
Arabidopsis (Li et al. 2013c, Zhang et al. 2013), tobacco, pepper temperature tolerance by protecting PSII from inhibition owing
(Dang et al. 2013) and soybean (Chen et al. 2006, Zhu et al. to high ROS in transgenic tobacco (Yang et al. 2007); similarly,
2006b). Similarly, over-expression of HSP and related genes was the presence of NADP (H) in leaf chloroplast pacifies the ROS
also reported in rice (Katiyar-Agarwal et al. 2003), maize activity under HS in transgenic tobacco (Wang et al. 2006).
(Nieto-Sotelo et al. 2002), carrot (Malik et al. 1999), Arabidopsis Over-expression of maize acetylcholine esterase AChE gene
(Prandl et al. 1998, Panchuk et al. 2002, Rhoads et al. 2005, in transgenic tobacco evidenced its role in HS tolerance
Heat stress in crop plants
(Yamamoto et al. 2011, Yamamoto and Momonoki 2012). In
cotton, engineering of AtSAP5-encoding proteins having A20/
AN1 zinc finger domains prohibited damage in photosystem
(PS) II complex under HS (Hozain et al. 2012). The involvement
of isoprene in providing HT was documented in transgenic Ara-
bidopsis expressing isoprene synthase gene from Populus alba
(Sasaki et al. 2007) and was also very well characterized in
transgenic tobacco (Vickers et al. 2009). Enhanced HT was also
credited to increased expression levels of cytokinin oxidase/
dehydrogenase (CKX) gene in transgenic tobacco (Mackov
a
et al. 2013) and sedoheptulose-1, 7-bisphosphatase (SBPase)
gene in transgenic rice (Feng et al. 2007).
Taken the role of antioxidants into account, HvAPX1 gene
was introduced into Arabidopsis from barley, which later pro-
duced ascorbate, thus imparting HT (Shi et al. 2001). The loss-
of-function mutants in O. sativa glycogen synthase kinase3-like
gene 1 (OsGSK1) gene created by T-DNA insertion conferred
HT in rice (Koh et al. 2007). The cross-species gene transfer
offering HS tolerance is well exemplified in tobacco by trans-
ferring DnaK1 gene from a halo-tolerant cyanobacterium
(Aphanothece halophytica) (Ono et al. 2001). Likewise, transfer
of codA gene from Arthrobacter globiformis to tomato evinced
tolerance to HS during germination by enhancing expression of
several proteins including the mitochondrial small heat-shock
protein (MT-sHSP), heat-shock protein 70 (HSP70) and heat-
shock cognate 70 (HSC70) (Li et al. 2011). Expression of rice
gene ZFP177 and A20/AN1-type zinc finger gene provided HT
in tobacco (Huang et al. 2008). Recently, over-expression of
chloroplast-targeted DnaJ protein (LeCDJ1) gene also imparted
HT in transgenic tomato (Kong et al. 2014). To our
knowledge, the major research on transferring the HT genes is
invested so far in the model plants such as Arabidopsis,
tobacco and rice. Therefore, the next priority should be to
extend these technologies to the other agriculturally relevant
field crops.
Prospective role of precise and high-throughput
phonemics facilities
The continued progress in the new-generation high-throughput
DNA sequencing technologies permits generation of enormous
sequence information at acceptable prices (Feuillet et al. 2010,
Xu et al. 2012, Bevan and Uauy 2013). However, large-scale
phenotypic evaluation of crop plants, that is, precise, accurate
and high-throughput phenotyping of the traits, remains strenuous
(Cobb et al. 2013), in particular the phenotypic assessment of
yield/component traits and abiotic stress-tolerance-related traits,
which are under the control of complex network involving
QTLs, their epistatic interactions and strong G 9 E interactions
(Houle et al. 2010, Sozzani and Benfey 2011, White et al. 2012,
Cobb et al. 2013). Taking into account the environment as such
(as described by Xu et al. 2012), the accurate assessment of the
magnitude of G 9 E interactions by E-typing will transform the
selection procedures from being mere technical (phenotype
based) to much more scientific, which would consider all three
dimensions (genotype, phenotype and environment), that is, a
point-to-space transformation. In this way, by effectively control-
ling the environmental factors and errors, plant phenomics holds
the opportunity to understand the gene function, their response
to external environment and subsequently, bridging the gap
between genotype and phenotype by facilitating phenotyping of
important quantitative traits (Furbank 2009, Furbank and Tester
2010, Sozzani and Benfey 2011, Chen et al. 2014). Since the
13
establishment of Australian Plant Phenomics Facility (APPF) in
Australia (Finkel 2009), new avenues are being provided to
overcome the phenotyping bottlenecks.
To facilitate more realistic evaluation of the plant responses to
environment, field-based phenotyping (FBP) approaches are initi-
ated (White et al. 2012). Some of the remarkable large-scale
phenotyping techniques applied recently for screening against
abiotic stress are infrared thermography that efficiently captures
the genetic variability for stomatal response against water deficit
in wheat and barley (Munns et al. 2010) and stomatal behaviour
and canopy temperature in potato (Prashar et al. 2013). Infrared
thermography, an effective non-invasive tool, has been deployed
for phenotyping of HT in wheat and chrysanthemum (Amani
et al. 1996, Janke et al. 2013, Prashar and Jones 2014). Addi-
tionally, higher value of chlorophyll fluorescence parameter Fv/
Fm was observed in wheat, which reflected maximum efficiency
of PSII higher photosynthesis rate, higher stomatal conductance
and transpiration rate under HS (Sharma et al. 2014b). Further,
the above parameter was also used in assessment of genetic vari-
ability for HS tolerance in wheat (Sharma et al. 2012, 2014b).
Other strategies such as measuring canopy temperature were also
implemented for identifying high-yielding HS-tolerant wheat
lines with lower canopy temperature (Pinto et al. 2010, Mason
and Singh 2014). More recently, high-resolution thermal imaging
system was used to precisely measure the leaf temperature
(Jones and Sirault 2014). In recent years, various platforms were
established for phenotyping, including HTpheno for image
analysis (Hartmann et al. 2011), PHENOPSIS DB to perform
image analyses under different environmental conditions in Ara-
bidopsis (Fabre et al. 2011), Gia Roots for root architecture
analysis (Galkovskyi et al. 2012) and Phenoscope for spatial
homogeneity (Tisne et al. 2013). Rootscope represents another
phenotyping system that is recently used to quantify heat-shock
responses in plants (Kast et al. 2013). Excellent reviews were pub-
lished in recent years describing applications, benefits and chal-
lenges of the new-generation phenotyping systems (Sozzani and
Benfey 2011, Cobb et al. 2013). In the coming future, the new-
generation phenomics platforms would allow cost-effective and
user-friendly yet phenome-level screening for HT in crop plants.
Conclusion and prospects
Given the rising demands for global food supply coupled with
the severe pressure of population growth and the climate change
trajectories, strategies should mainly aim at proper exploration of
germplasm and harnessing of novel alleles from wild gene pool.
Moreover, the adaptive as well as morpho-physiological traits
could be incorporated in high-yielding genotype through physio-
logical trait breeding. In parallel, paradigm shift in molecular
marker systems coupled with growing availability of the whole-
genome sequences and rapid progress in functional genomics
can expedite the discovery of candidate gene conferring HT and
their genome-scale expression profiling. Moreover, transgenic
approaches hold great promise for transferring HS-tolerant genes
across the species. In addition, the hurdle of phenotyping of this
complex trait can be overcome by testing genotypes harbouring
HT under both stress and non-stressed condition along with
multilocation testing. Phenomics platforms raise new hope for
difficult-to-measure component traits associated with HT. Addi-
tionally, omics approaches combined with system biology
approach could greatly strengthen the conventional breeding to
mitigate the challenges of HS and to streamline the future of sus-
tainable agriculture (Ahuja et al. 2010, Cramer et al. 2011).
14
Acknowledgements
Authors acknowledge support from Indian Council of Agricultural
Research (ICAR), India.
Conflict of interest
The authors declare that there is no conflict of interest.
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