Increasing Rice Grain Yield Under Abiotic Stresses: Mutagenesis, Genomics and Transgenic Approaches

Abstract

Rice is a main source of food to millions of people across the world, and hence increase in its production/yield is vital to feed the rapidly growing population. However, the yield of rice is decreased to a large extent due to the adverse effects of several kinds of abiotic stresses such as drought, salinity, heat stresses, etc. Different traditional and modern breeding approaches have been used to mitigate the damaging effects of different abiotic stresses on rice production. Traditional breeding strategies such as hybridisation and selection have resulted in the development of few stress-tolerant varieties, but such strategies are laborious and time-consuming. The modern biotechnological approaches such as mutagenesis, transgenics and genomics have been effective in the identification, cloning and characterisation of genes that govern tolerance to different abiotic stresses. Insertion of such genes into the rice plants have decreased the yield loss caused by various abiotic stresses. Modern biotechnological tools have brought landmark achievements by developing varieties with enhanced tolerance to various abiotic stresses. The role of mutagenesis, genomics and transgenic approaches in the creation of rice varieties with improved yield under different abiotic stress has been reviewed in this chapter.

Full text

Increasing Rice Grain Yield Under Abiotic
Stresses: Mutagenesis, Genomics
and Transgenic Approaches
Aamir Raina, Samiullah Khan, Parmeshwar K. Sahu, and Richa Sao
Abstract
Rice is a main source of food to millions of people across the world, and hence
increase in its production/yield is vital to feed the rapidly growing population.
However, the yield of rice is decreased to a large extent due to the adverse effects
of several kinds of abiotic stresses such as drought, salinity, heat stresses, etc.
Different traditional and modern breeding approaches have been used to mitigate
the damaging effects of different abiotic stresses on the rice production. Tradi-
tional breeding strategies such as hybridisation and selection have resulted in the
development of few stress-tolerant varieties, but such strategies are laborious and
time-consuming. The modern biotechnological approaches such as mutagenesis,
transgenics and genomics have been effective in the identification, cloning and
characterisation of genes that govern tolerance to different abiotic stresses.
Insertion of such genes into the rice plants have decreased the yield loss caused
by various abiotic stresses. Modern biotechnological tools have brought land-
mark achievements by developing varieties with enhanced tolerance to various
abiotic stresses. The role of mutagenesis, genomics and transgenic approaches in
the creation of rice varieties with improved yield under different abiotic stress has
been reviewed in this chapter.
A. Raina (*)
Mutation Breeding Laboratory, Department of Botany, Aligarh Muslim University, Aligarh, Uttar
Pradesh, India
Botany Section, Women’s College, Aligarh Muslim University, Aligarh, Uttar Pradesh, India
S. Khan
Mutation Breeding Laboratory, Department of Botany, Aligarh Muslim University, Aligarh, Uttar
Pradesh, India
P. K. Sahu · R. Sao
Department of Genetics and Plant Breeding, Indira Gandhi Agriculture University, Raipur,
Chhattisgarh, India
#Springer Nature Singapore Pte Ltd. 2020
A. Roychoudhury (ed.), Rice Research for Quality Improvement: Genomics
and Genetic Engineering,https://doi.org/10.1007/978-981-15-4120-9_31
753

Keywords
Drought · Heat · Salinity · Mutagenesis · Transgenics · Genomics
1 Introduction
Oryza sativa L. is commonly known as rice with chromosome complement
2n¼2x¼24, a member of Poaceae family with a huge diversity comprising of
more than 40,000 cultivated varieties. Rice is an ancient staple food with the origin
of centre in southern and south-western tropical Asia and origin of domestication in
India and China (Vavilov 1926). Oryza sativa is the main species of rice cultivated
across the world. To date, 23 species and ten kinds of genomes of rice including AA,
BB, CC, BBCC, CCDD, EE, FF, GG, HHJJ and HHKK have been reported
(gramene.org). About one in three persons on Earth consumes rice, and it is believed
that more than 50% of total human population is dependent on rice for their food
requirements. According to FAO forecasts, the food production must be double to
feed the rapidly growing human population which is likely to rise to nine billion in
2050. In addition to sky high population; shrinking arable land, depleating natural
resources, erratic rainfalls and drastic climate change further reduces the rice pro-
duction. This will create a huge demand on the food production and will exceed the
food supply by a greater mark. Further, the overall yield of rice is sternly reduced by
several environment induced abiotic stresses (Ansari et al. 2015; Manju et al. 2017).
Increasing population and economic development have been posing a growing
pressure for increase in food production (Zhang 2007). All these challenges can be
met by the development of rice varieties with improved yield, resistance to abiotic
stresses and improvement in grain quality via the use of modern biotechnological
breeding approaches (Fahad et al. 2016a,b).
1.1 Abiotic Stresses
The occurrence of global warming, depleting rice lands, exhausted water resources,
erratic rainfalls, expanding urbanisation and climate-induced abiotic stresses lead to
significant reduction in the production of crops including rice (Pandey et al. 2015,b).
Among the abiotic stresses, drought, salinity and heat have been reported to cause
substantial yield loss in various agro-economically important crops (Ahmad and
Samiullah 2019; Ahmad et al. 2019). In the current scenario, it is imperative to
employ breeding approaches both conventional and modern with the main aim of
increasing tolerance to abiotic stresses (Leonforte et al. 2013). However, with the
complex nature of inheritance of tolerance to abiotic stress and meagre understand-
ing, it will be quite difficult to enhance tolerance in existing rice varieties (Lafitte
et al. 2006). The main abiotic stresses that limit the rice production are discussed
below.
754 A. Raina et al.

1.2 Drought Stress
As compared to other cereals, rice requires a huge quantity of water to complete its
life cycle (Pandey and Shukla 2015). The drought reduces the yield, and the degree
of reduction depends on the variety and the timing of drought occurrence
(Wassmann et al. 2009; Dixit et al. 2014a,b). In addition to yield reduction, the
drought stress affects various morpho-physiological and biochemical traits in rice
plants (Basu et al. 2010). The significant decline in crop yield has been attributed to
the negative impact of drought on plant growth, physiology and reproduction. Nahar
et al. (2016) reported that drought induced low seed germination and decreased
seedling growth could be the probable reason for substantial yield drop. Drought
also disrupts the regulation of stomatal opening and closing by making stomatal
closure at higher rate, reduces leaf water potential and consequently leads to decrease
in cell dimensions and overall plant growth. The drought stress also causes a
reduction in leaf dimensions and turgor pressure within leaf cells which in turn
result in leaf rolling and quick senescence. An observation of reduced cell division
and root elongation on the onset of drought may be attributed to the lesser growth
and yield of the plant (Singh et al. 2012). Furthermore, severe drought stress results
in drop in photosynthetic and respiration rate, translocation and ion uptake and
carbohydrate and nutrient metabolism and consequently leads to stunted growth
(Jaleel et al. 2008; Razmjoo et al. 2008). In addition to the abovementioned effects,
drought stress also causes disturbance in assimilate partitioning and photosynthetic
rate which eventually lead to a considerable reduction in overall yield (Praba et al.
2009). A shrink in the photosynthetic rate also results in reduced activity of
chlorophylls a and b, PSI, PSII and photosynthetic enzymes such as Rubisco and
PEPcase, thus reducing the rate of carbon dioxide fixation and overall production
(Asharf and Harris 2013; Banerjee and Roychoudhury 2018). In order to combat the
devastating effects of drought on plant growth and development, it is imperative to
have broader understanding of drought stress and its tolerance mechanism (Nahar
et al. 2016).
1.3 Heat Stress
In the era of global warming due to continuous increase in the atmospheric
temperatures, heat stress is considered as a potential abiotic stress that limits the
overall yield of many agro-economically important crops including rice (Fahad et al.
2017). Rice is more sensitive to the heat stress occurring at grain filling stage that
adversely affects many physiological and biochemical processes in crop plants,
which result in reduced plant productivity (Zhang et al. 2016). Apart from various
negative effects of heat stress on the grain filling stage, vegetative parts are also
greatly impacted due to heat stress, and its impact depends on the variety grown and
timing of occurrence. It also induces a series of morpho-physiological and biochem-
ical variations, especially in enzyme activities with abnormal elevation or complete
denaturation which consequently affects the overall growth. Heat stress also causes
Increasing Rice Grain Yield Under Abiotic Stresses: Mutagenesis, Genomics and... 755

reduction in pollen fertility, thereby disrupting the pollination rate, and hence
reduced flower and seed set. This has been attributed to substantial decrease in
yield in rice (Zhang 2007; Liu et al. 2013). Heat stress at the flowering stage resulted
in the increase in the number of sterile and aborted spikelet that leads to a drop in
yield, while heat stress at harvesting stage did not affect overall yield (Aghamolki
et al. 2014). Fahad et al. (2016c) have reported that elevated temperature at night also
results in a reduction in 100-grain weight, which is considered as one of the main
yield-attributing traits of rice.
1.4 Salinity Stress
Globally, salinity stress is recognised as one of the most devastating abiotic stresses
that limit the overall crop production of cereals (Mondini and Pagnotta 2015). It is
considered as one of the main obstacles in achieving the desired goals of rice
production as the rice varieties are more sensitive to the salinity stress that incurs
more than 50% yield loss. Therefore, attention needs to be paid towards the genetic
improvement of rice varieties with improved tolerance to salinity (Molla et al. 2015).
All the main developmental stages including germination, vegetative, flowering and
seed stages are influenced by the increase in salinity stress (Fujino et al. 2004). The
effectiveness of employing a proper selection of rice seedlings for the development
of rice varieties with improved salt tolerance and subsequent increase in the overall
yield and yield-attributing traits has been reported by Cuartero et al. (2006). How-
ever, traditional breeding approaches such as selection is cumbersome, laborious and
time-consuming and would require 8–9 years on an average for the development and
official release of salt-tolerant rice varieties. Therefore, to speed up the development
of elite varieties, it is important to have an in-depth understanding of mechanism
underlying salinity tolerance at morpho-physiological and molecular levels
(Roychoudhury et al. 2008; Horie et al. 2012). Baby et al. (2010) have reported
that the development of salinity-tolerant genotypes is a challenging task as the
salinity tolerance is polygenic trait with complex mode of inheritance; therefore,
direct selection for tolerance trait is rarely effective. Hence, to create rice varieties
with improved salt tolerance, deeper research that is based on identifying key genes
that govern the inheritance of salt tolerance trait is required (Bizimana et al. 2017).
Several morphological and molecular markers should be employed to screen and
select the rice seedlings that display high tolerance to salt stress. After screening, the
rice seedlings should be subjected to multi-location trials to check the stability of
tolerance trait before official release of salt-tolerant rice varieties (Roychoudhury
and Chakraborty 2013).
756 A. Raina et al.

2 Modern Breeding Approaches for Improving Abiotic Stress
Tolerance in Rice
At present, efforts are made to identify key genes that play a critical role in the
abiotic stress tolerance with the main objective of creation of rice varieties with
improved stress tolerance. For this, several approaches have been used from time to
time, and some of the main approaches include mutagenesis, genomics, transgenics,
etc. (Kim et al. 2014; De Leon et al. 2017; Okazaki and Saito 2016; Manju et al.
2017). However, transgenics and genomics were more successful in developing the
varieties with improved tolerance to a wide range of abiotic stresses and are
discussed in detail in following subsections.
2.1 Mutagenesis
Induced mutations by chemical and/or physical agents were employed by several
plant breeders to create rice varieties with high yielding potential and better tolerance
to abiotic stress (Raina et al. 2016; Khursheed et al. 2019). The continuous use of
traditional breeding approaches in the past several decades led to narrowing of
genetic variation in several crops including rice. Among the various breeding
approaches used to date, mutagenesis has proven relatively effective tool for
enhancing the genetic variation and improving resistance to abiotic stresses. Muta-
genesis equips the plant breeders to make the efficient selection of the genotype for
the desired traits including resistance to abiotic stresses (Raina et al. 2018a; Raina
and Danish 2018). Several researchers have employed different mutagens in differ-
ent doses for creating varieties with desired traits in crops such as chickpea (Laskar
et al. 2015; Raina et al. 2017, Raina et al. 2019), lentil (Laskar et al. 2018a,b),
cowpea (Raina et al. 2018b), mung bean (Goyal et al. 2020a,b; Wani et al. 2017),
faba bean (Khursheed et al. 2018a,b, Khursheed et al. 2018c), fenugreek (Hassan
et al. 2018) and black cumin (Amin et al. 2016,2019; Tantray et al. 2017).
Mutagenesis has played a vital role in improving characters such as plant yield,
earliness, adaptability and tolerance to a wide range of abiotic stresses (Khursheed
et al. 2015,2016; Laskar et al. 2019; Goyal et al. 2019a,b; Raina and Khan
2020; Raina et al. 2020).
At present, continuously rising global warming along with drastic climate change
has led to increased occurrence of drought which is affecting the overall production
of important crops such as rice (Hallajian 2016). The International Rice Functional
Genomics Consortium maintains 0.2 million mutant lines of rice, with mutations in
about 50% of mapped genes to date (Krishnan et al. 2009). The FAO/IAEA Mutant
Variety Database (MVD) maintains information about 3322 officially released
mutant varieties which include 829 rice mutant varieties (www.mvd.iaea.org
accessed March 2020). Recently in April 2019, a mutant variety of rice named as
‘Trombay Chhattisgarh Dubraj Mutant-1’has been developed and released in
Chhattisgarh, India. This variety has short stature and early maturity which improved
its resistance to lodging and the grain yield. Several drought-tolerant rice varieties
Increasing Rice Grain Yield Under Abiotic Stresses: Mutagenesis, Genomics and... 757

have been created all over the world. In 2015, two drought-tolerant rice mutant
varieties named as NMR 151 and NMR 152 have been developed by irradiation of
popular Malaysia rice variety MR 219 (breeding line developed by MARDI) using
gamma rays at dose 300 Gy (mvd.iaea.org accessed March 2020).
Up to now, nine drought-tolerant varieties of rice, viz. 202 in 1973 at China,
Azmil mutant in 1976 at Philippines, RD 15 in 1978 at Thailand, CNM 6 in 1982 at
India, Danau atas in 1988 at Indonesia, IACuba 23 in 1995 at Cuba, NMR 151 in
2015 at Malaysia, NMR 152 in 2015 at Malaysia and Binadhan-19 in 2017 at
Bangladesh, have been developed (Table 1). Researchers at Vienna promote creation
of more sustainable rice varieties with the main aim to improve the tolerance to
abiotic stresses such as drought, heat and salt stress (Kaskey 2013). India made a
landmark achievement by developing a mutant variety of rice, viz. CNM
6 (Lakshmi), by irradiating IR8 with 300 Gy X-rays under real field conditions at
different geographical sites with improvement in tolerance to drought, reduction in
maturity and stature and enhancement in aroma and yield (mvd.iaea.org accessed
March 2020). Researchers at Australia were successful in developing rice varieties
with improved tolerance to abiotic stresses and enhanced grain yield. Another
mutant Nagina 22 (N22) was developed by treating the parent variety with ethyl
methanesulfonate; the mutant variety displayed improvement in a deep-rooted
system and enhanced tolerance to drought and heat stress (Panigrahy et al. 2011).
Heat stress is also one among the major abiotic stresses that restricts plant growth,
metabolism and overall production of plants worldwide (IPCC 2007). Heat stress
influences all growth stages of rice and incurs a huge loss in rice grain quality and
yield (Nakagawa et al. 2003; Matsui et al. 1997). Mutagenesis is used to increase the
overall genetic variability of rice that enables the rice breeders to make selection for
the heat stress-tolerant lines. Physical mutagens such as gamma rays have broaden
the scope of increasing genetic variability in various agro-economic traits. Gamma
radiations were employed by rice breeders to improve genetic variations and to
render them more yielding and tolerant to heat stress (Luzi-Kihupi et al. 2009). The
rice mutant varieties may involve heat resistance mechanism that is linked with
increased synthesis and build-up of heat shock proteins. However, the molecular
mechanism making rice plant cells survive from heat stress is very complicated, and
hence more information is needed. The heat-resistant mutant variety, namely,
Zaoyeqing, was developed by irradiation of seeds with 200 Gy gamma rays and
officially approved in 1980. Another mutant variety named as Binadhan-14 was
developed in 2013 by Bangladesh. This variety had improved tolerance to high
temperature, shorter height and long fine grains (mvd.iaea.org accessed March
2020). The mutant rice lines were developed using 150 and 200 Gy gamma rays
with the main aim of enhancing tolerance to heat stress. Recently, Targeting Induced
Local Lesions in Genome (TILLING), a reverse genetic method, has been used for
the characterisation of putative heat-tolerant (HT) mutant upland rice lines from
gamma ray-induced mutation and target mutation in genes linked with heat stress
tolerance. Although originally TILLING was developed for use with Arabidopsis
only, now the technique has been applied to a wide range of plants, including rice
(Till et al. 2006). McCallum et al. (2000) reported its use for detection of mutations
758 A. Raina et al.

Table 1 Role of mutagenesis in the development of rice varieties with enhanced tolerance to
abiotic stresses (MVD 2019)
Name Country Year
Mutagen
(dose) Traits improved
202 China 1973 Gamma rays
(200 Gy)
Small leaves, large panicle and
tolerance to drought
CNM 6 India 1980 X-rays
(300 Gy)
Early maturity, increased tillering,
10% higher yield, long grain size,
resistance to drought, dwarf (85 cm),
long bold grains
Danau atas Indonesia 1988 Gamma rays
(400 Gy)
Resistance to drought, high yield
RD 15 Thailand 1978 Gamma rays
(150 Gy)
Early maturity and tolerance to drought
Azmil
mutant
Philippines 1976 Gamma rays
(200 Gy)
High yield, drought resistance
IACuba 23 Cuba 1995 Fast neutrons
(20 Gy)
Resistance to drought and high
amylose content
Binadhan-19 Bangladesh 2013 Physical
mutagen
Shorter height, shorter duration,
uniform plant growth, long and slender
grains with golden colour, higher yield
NMR 151 Malaysia 2015 Gamma rays
(300 Gy)
Minimal water requirement and high
yield
NMR 152 Malaysia 2015 Gamma rays
(300 Gy)
Minimal water requirement, high yield
and longer panicle length
Zaoyeqing China 1980 Gamma rays
(200 Gy)
Large panicle and tolerance to high
temperature
Fuxuan 1 China 1968 Gamma rays
(300 Gy)
Early maturity, tolerance to salinity
and good adaptability
Liaoyan 2 China 1992 Gamma rays Tolerance to salinity, high yield,
multiple resistance, high quality, good
adaptability
Rasmi India 1976 Gamma rays
(220 Gy)
Awnless, high yield, tall plant type and
tolerance to salinity
Mohan India 1983 Gamma rays Salt tolerance
Atomita 2 Indonesia 1983 Gamma rays
(200 Gy)
Tolerance to salt, early maturity,
higher protein content
Shadab Pakistan 1987 0.5% EMS High yield, improved grain quality,
resistance to salinity
Shua 92 Pakistan 1993 Gamma rays Resistance to salinity and high yield
NIAB-IRRI-
9
Pakistan 1999 Fast neutrons
(15 Gy)
Salt tolerance
A-20 Viet Nam 1990 0.015%
MNH
Early maturity and high tolerance to
salinity
DT17 Viet Nam 1999 NA High yield and tolerance to salinity
VND 95-19 Viet Nam 1999 Gamma rays
(200 Gy)
Strong tolerance to acid sulphate soil,
sturdy stem, high yield (5–10 t/ha)
(continued)
Increasing Rice Grain Yield Under Abiotic Stresses: Mutagenesis, Genomics and... 759

in rice genomes; TILLING method can be used to screen genes for specific
mutations using a PCR assay and then enzymatic digestion of PCR products by
CEL I (Till et al. 2006). Among the 64 putative rice lines screened for heat tolerance,
34 mutant rice lines were recognised to have mutations in heat-tolerant genes (HSP
genes) and reflected enhanced tolerance to high temperatures (Yona 2015).
Mutagenesis technique also played a vital role in developing crop varieties with
improvement in tolerance to salinity stress. To date, about 15 mutant varieties with
enhanced tolerance to salt stress have been developed. Moreover, there are several
other elite mutants that showed promising results for heat tolerance and are subjected
to multi-location trials as a prerequisite for the official registration and release. The
rice mutant, viz. Shu-92, developed in Pakistan showed substantial increase in yield
by 40–49% margins against standard salt-tolerant checks (Balooch et al. 2003).
Another rice mutant, GINES, has been developed in 2007 by Cuba which have
reflected high tolerance to saline soils and higher yielding potential. Bangladesh
Institute of Nuclear Agriculture (BINA) in collaboration with International Rice
Research Institute (IRRI) has been successful in developing two salt-tolerant rice
varieties, namely, BINA dhan 8 and BINA dhan 10, which showed substantial
improvements in tolerance to salt stress (bina.gov.bd). The collaborative mutagene-
sis research between the IAEA and IRRI aimed at the genetic improvement of rice
with the focus on improving salt tolerance in the backdrop of increased salt concen-
tration in rice lands. A major breakthrough was the development of salt-tolerant
variants from IR29, a variety which is highly sensitive to salt stress. The salt-tolerant
mutant lines derived from IR29 with improved traits will play a major role in
addressing the scourge of salinity in rice agriculture in Southeast Asia (Mba et al.
2007). Further attention has been paid towards the improvement for the overall plant
growth and development and grain quality and quantity of wild rice species, Pokkali
(Lee et al. 1996; Gregorio et al. 2002).
Table 1 (continued)
Name Country Year
Mutagen
(dose) Traits improved
VND 95-20 Viet Nam 1999 Gamma rays
(200 Gy)
Short duration (90–95 days), stiff stem,
high yield, amylose content, tolerant to
salinity
Lunisree India 1992 NA Long slender grain for coastal saline
areas, high yield
GINES Cuba 2007 The mutant
variety
protons
(20 Gy)
Tolerance to salinity and good quality
Wonhaebyeo Korea,
republic of
2007 Gamma rays
(50 Gy)
Tolerance to salinity
760 A. Raina et al.

2.2 Transgenics
The abiotic stresses incurred a huge loss to the overall productivity of rice, and
common transgenic approaches are employed to address the issues of abiotic stress
(Table 2). As the understanding of mechanisms involved in tolerance to abiotic
stresses increases, the identification and characterisation of multiple genes that
govern the stress tolerance is becoming easier. In response to salinity, drought and
heat stress plants regulate the expression of genes that control the synthesis of low
molecular weight compounds, viz. GB (glycine betaine), proline, trehalose, ampho-
teric quaternary amines and LEA (late embryogenesis abundant) proteins to combat
the effects of abiotic stresses (Roychoudhury et al. 2011; Roychoudhury et al. 2015;
Roychoudhury and Banerjee 2016). Shirasawa et al. (2006) reported the increased
synthesis of GB that imparted resistance to salinity and heat stress in transgenic rice
overexpressing spinach choline monooxygenase. Kumar et al. (2009) have reported
mutagenised gene P5CS (Δ
1
-pyrroline-5-carboxylate synthase) with phenylalanine
substituted for an alanine at 129-amino acid position, hence named as P5CSF129A
gene in transgenic rice that leads to the increased synthesis of proline in response to
exposure to salinity stress. Similarly, another gene in transgenic rice that plays a vital
role in imparting tolerance to abiotic stress is OsTPS1 (trehalose-6-phosphate
synthase) and results into manifold increase in the synthesis of osmoprotectant
solute, proline and trehalose (Li et al. 2011). Xiao et al. (2007) and Duan and Cai
(2012) have reported that overexpression of OsLEA3-2 (rice late embryogenesis
abundant), OsLEA3-H and OsLEA3-S genes in genetically engineered rice imparted
much better resistance to drought and salt stress. The role of polyamines in combat-
ing the abiotic stresses is not much known and is at very initial stage; however, the
functional genomics have brought few significant insights into the role of polyamine
synthesising genes in abiotic stress tolerance. Although no genetically engineered
rice with increased polyamine synthesis have been developed, however, preliminary
research has reflected that genes OsPUT1 (rice polyamine uptake transporter) and
AdoMetDC (S-adenosylmethionine decarboxylase) are the potential candidate genes
that confer the tolerance to abiotic stresses via regulating the synthesis of polyamine
(Mulangi et al. 2012). To date, a huge number of transcription genes have been
isolated and characterised that confer resistance to drought, heat and salinity (Kumar
et al. 2013). Many genes isolated from different plants or even rice varieties that
show tolerance to abiotic stresses have been introduced into widely cultivated rice
varieties through genetic modification with the objective to enhance the tolerance to
a wide range of abiotic stresses. Some of the noteworthy examples include the
following: The transgenic rice showing overexpression of HvCBF4, ZmCBF3,
OsDREB1F and OsDREB2A isolated from barley, maize and rice, respectively,
introduced and overexpressed showed an increased survival under salinity and
drought stress (Wang et al. 2008,b; Mallikarjuna et al. 2011). Research has shown
that different transcription factors (TFs) in transgenic rice play a pivotal role in
modulating the expression of genes that govern the tolerance to a wide range of
abiotic stresses (Todaka et al. 2012).
Increasing Rice Grain Yield Under Abiotic Stresses: Mutagenesis, Genomics and... 761

Abscisic acid (ABA) is popularly known as stress hormone due to its critical role
in mitigation of a wide range of abiotic stresses. In rice varieties with improved stress
tolerance, ABA-synthesising gene is unregulated and led to increased synthesis of
ABA under stress conditions, and hence it is evident that ABA production is directly
Table 2 Role of transgenics in the development of rice varieties with enhanced tolerance to abiotic
stresses
Gene(s) Traits improved References
AtHsp101, OsHsp101 Heat tolerance Agarwal et al. (2003)
OsPIP1;3 Cold tolerance Lian et al. (2004)
Choline monooxygenase Salt and heat tolerance Shirasawa et al. (2006)
SsNHX1, AVP1 Salt tolerance Zhao et al. (2006a,b)
OsSBPase Heat tolerance Feng et al. (2007)
HvPIP2;1 Salt tolerance Katsuhara (2007)
OsGSK1 Heat tolerance Koh et al. (2007)
KatE Drought tolerance Nagamiya et al. (2007)
HvCBF4 Cold, drought and salt stress Oh et al. (2007)
OsLea1-3 Drought tolerance Xiao et al. (2007)
ZFP245 Cold tolerance Huang et al. (2009)
RWC3 Drought tolerance Matsumoto et al. (2009)
OsWKRY11 Heat and drought tolerance Wu et al. (2009)
OsTPS1 Cold, drought and salt stress Li et al. (2011)
OsNAC5 Cold, drought and salt stress Song et al. (2011)
ZmCBF3 Cold, drought and salt stress Xu et al. (2011)
ZmCBF3 Cold, drought and salt stress Xu et al. (2011)
OsMYB55 Heat tolerance El-kereamy et al. (2012)
OsCam1-1 Salt tolerance Saeng-ngam et al. (2012)
OsMYB48-1 Drought and salt stress Xiong et al. (2014)
GS2 Salt and cold tolerance Hoshida et al. (2000)
OsCDPK7 Salt and drought tolerance Saijo et al. (2000)
Adc, Samdc Salt and drought tolerance Capell et al. (2004)
HVA1 Salt and dehydration tolerance Babu et al. 2004
OtsA Salt, drought and cold tolerance Jung et al. (2004)
pdc1, adc Submergence tolerance Rahman et al. (2001)
AGPAT, SGPAT Cold-tolerant Ariizumi et al. (2002)
Cat Cold-tolerant Matsumura et al. (2003)
spl7 Tolerance to heat stress Yamanouchi et al. (2002)
OsPYL3 and OsPYL9 Drought and cold tolerance Tian et al. (2015)
SOD2 Salt tolerance Zhao et al. (2006a,b)
P5CS Salt tolerance Karthikeyan et al. (2011)
MnSOD Drought tolerance Wang et al. (2005)
pENA1 Salt tolerance Jacobs et al. (2011)
miR319 Cold, salt and drought tolerance Khraiwesh et al. (2012)
762 A. Raina et al.

related to enhanced stress in rice (Roychoudhury and Paul 2012). With the increas-
ing understanding of ABA-mediated signalling pathways, several bZIP TFs have
been discovered to play a key role in drought stress tolerance, thereby improving the
yield substantially (Banerjee and Roychoudhury 2017; Kumar et al. 2019). Saeng-
ngam et al. (2012) have reported that MAPK (mitogen-activated protein kinase) and
Ca
2+
/CaM (calcium/calmodulin)-mediated pathways play a crucial role in stress
signalling response. Several novel genes have been isolated and characterised by
working on these pathways. For instance, OsCam1-1 (rice calmodulin gene) can
sense the severity of salt stress and upregulate the ABA synthesising gene to build up
more ABA which in turn impart increased tolerance to salinity (Saeng-ngam et al.
2012). Another gene OsMAPK44 (rice mitogen-activated protein kinase) has been
shown to play a critical role in the mitigation of various abiotic stresses, particularly
salinity and drought (Jeong et al. 2006). Lee et al. (2011) while studying the role of
genes in stress signalling reported that downregulation of OsMAPK33 resulted in
the improvement of tolerance to salinity stress in rice plants. Nagamiya et al.
(2007,b) and Gu et al. (2013) have reported that several genes such as KatE
(E. coli catalase), OsIRL (rice isoflavone reductase-like gene), PPDK (maize pyru-
vate orthophosphate dikinase) and PEP carboxylase (maize phosphoenolpyruvate
carboxylase) introduced and overexpressed increased the survival of rice plants
exposed to drought and salt stress. Several workers have postulated different under-
lying mechanisms that confer tolerance to salinity stress, and one such mechanism
has been attributed to the upregulation of Na/H (sodium proton pump) gene that led
to rapid and effective extrusion of sodium ions across the cell membranes. Another
gene, viz. SOD2, (superoxide dismutase) isolated from fission yeast and introduced
and overexpressed into rice imparted substantial increase in the rate of photosynthe-
sis, increased grain yield and improved salt tolerance (Zhao et al. 2006a,b). The
genetically engineered rice with overexpressed (Na
+
pumping ATPase gene)
PpENA1 isolated from moss Physcomitrella patens revealed enhanced potential to
withstand salt stress (Jacobs et al. 2011). Similarly, the OsECS (γ-glutamylcysteine
synthetase) gene overexpression in genetically engineered rice showed enhanced
seed germination and seedling survival in rice exposed to abiotic stress, and this has
been attributed to improved redox homeostasis (Choe et al. 2013). In addition to the
genes, several micro-RNAs, for instance, miR160, have been reported to play a
critical role in mitigation of adverse effects of drought stress in rice (Nadarajah and
Kumar 2019).
Apart from the transcription factors and signalling pathways, aquaporins,
members of the major (membrane) intrinsic protein (MIP) family, have been
reported to play a role in improving the ability to tolerate salt and drought stress.
For instance, transgenic rice harbouring and/or overexpressing HvPIP2;1 (barley
aquaporin gene), OsPIP1;1 (rice aquaporin gene) and RWC3 (rice water channel
protein) plays an important role in imparting tolerance towards salinity and drought,
respectively (Kapilan et al. 2018). Zhao et al. (2006a,b) while studying salt tolerance
in rice reported that co-expression of SsNHX1 (vacuolar Na+/H+ antiporter gene)
and AVP1 (vacuolar H+-PPase) isolated from Suaeda salsa and Arabidopsis,
respectively, introduced in transgenic rice seedlings revealed improved tolerance
Increasing Rice Grain Yield Under Abiotic Stresses: Mutagenesis, Genomics and... 763

to salinity with increased grain yield. Genetically engineered rice plants harbouring
and overexpressing ZFP245 displayed substantial increase in tolerance to drought
and other abiotic stresses (Huang et al. 2009). Further, the increased stress tolerance
has been attributed to augmented proline content and upregulation of P5CS and
proline transporter genes. Likewise, another gene PgNHX1 (vacuolar Na+/H+
antiporter) isolated from Pennisetum glaucum and introduced in transgenic rice
showed enhanced plant yield in severe salt stress (Verma et al. 2007). The literature
is scanty on identification, isolation and characterisation of transporter genes and
underlying mechanism that impart stress tolerance in rice. More attention is required
to pay toward this area to develop a broader understanding of the role of transporter
genes in conferring tolerance to abiotic stress (Huang et al. 2009).
Several new genes such as Athsp101 (Arabidopsis heat shock protein), FAD7
(Arabidopsis thaliana fatty acid desaturase) and OsHSP101 (rice heat shock protein)
governing the heat tolerance serve as a promising approach in developing transgenic
rice plants with increased yield under heat stress. Transgenic rice revealed manifold
increase in heat tolerance due to downregulation of FAD gene (Sohn and Back
2007). These genes required for acclimation to heat stress and their insertion into rice
resulted into the development and official release of heat-tolerant rice varieties
(Agarwal et al. 2003). The knockout mutants of OsGSK1 gene showed substantial
increase in the ability to tolerate high temperature (Koh et al. 2007). Likewise, the
upregulation of SBPase gene imparted heat tolerance along with the simultaneous
increase in grain yield due to increased rate of carbon dioxide fixation in genetically
engineered rice plants (Feng et al. 2007). Additionally, the upregulation of
OsMYB55 (rice myb transcription factor 55) activates stress genes associated with
increased heat tolerance, amino acid metabolism and grain yield in transgenic rice
(Deeba et al. 2017).
2.3 Genomics
To feed the rapidly increasing human population, creation of varieties with high
yielding potential and improved resistance towards abiotic stresses is prerequisite
(Leonforte et al. 2013). Chee et al. (2005) have documented that conventional
approaches of breeding such as mutagenesis are cumbersome and require a longer
time span; modern breeding strategies such as marker-assisted breeding (MAB) have
proven effective for creating varieties with enhanced yield and stress tolerance in a
short span of time with better precision. MAB has been employed in several
agricultural and horticultural important crops in rice with the objective to screen
and isolate varieties with abiotic stress tolerance (Mondal et al. 2013). Molecular
markers, viz. RFLP, RAPD, AFLP, SSRs and SNPs have played a vital role in
marker-assisted breeding (MAB) for developing crops with improved tolerance to
abiotic stress (Hussain 2006; Raina et al. 2019). QTL mapping has been employed to
understand the underlying mechanism of abiotic stress tolerance in rice
(Shanmugavadivel et al. 2017).
764 A. Raina et al.

Increased salt concentration in the rice lands incurs a huge loss in overall yield
and monetary loss worldwide. In order to improve the yield in rice, it is important to
identify, isolate and characterise genes that improve acclimation to salt stress
(Table 3). Therefore, global collaborative research has been initiated with the main
objective of screening QTLs that govern improved salt stress tolerance in rice. Since
the tolerance to salinity is polygenic trait, it is difficult to screen QTLs that are linked
with salt tolerance and is at the central place in broadening the concept of stress
responses in a wide range of crops. A landmark achievement was made by develop-
ing a set of introgression lines (ILs) from “Pokkali”which served as donor of genes
that confer tolerance to salinity stress in a “Bengal”rice cultivar with better yield but
sensitive to mild salt concentration in soil. These ILs were subjected to genotyping
using SSRs and SNP markers and lead to the identification of 18 and 32 QTLs,
respectively, that are linked with salt stress tolerance and can be used to transfer
Table 3 Role of genomics in the development of rice varieties with enhanced tolerance to abiotic
stresses
Gene(s) Traits improved References
DSM1 Dehydration tolerance Ning et al. (2010)
OsCPK12 Salt tolerance Asano et al. (2012)
OsCPK4 Salt and drought tolerance Campo et al. (2014)
OsSIK1 Salt and drought tolerance Ouyang et al. (2010)
SIT1 Salt tolerance Li et al. (2014)
OsPP18 Osmotic and oxidative stress
tolerance
You et al. (2014)
OsANN1 Drought tolerance Qiao et al. (2015)
Os SAPK2 Drought tolerance Lou et al. (2017)
Dro1 Drought tolerance Uga et al. (2011)
Saltol Salt tolerance Das and Rao (2015)
qDTY2.2, qDTY3.1 and qDTY12.1 Drought tolerance Shamsudin et al.
(2016)
SKC1 Salinity stress Emon et al. (2015)
DST Salinity stress Emon et al. (2015)
qSCT-11 Chilling-tolerant Chen and Li (2005)
qPSST-3, qPSST-7, qPSST-9, qSCT1a
and qSCT2
Cold stress Jena et al. (2010)
qHTSF4.1 Heat stress Ye et al. (2015)
ABo28184 Drought tolerance Khattab et al. (2014)
AJ578494 Drought tolerance Khattab et al. (2014)
OsNAC2 Salt, drought, cold stress Hu et al. (2006)
OsDREB2A Salt, drought, cold stress Chen et al. (2008)
OsNAC5 Salt, drought, cold stress Hu et al. (2008)
OsHOX24 Salt, drought, cold stress Bhattacharjee et al.
(2017)
OsCMO Salinity stress Burnet et al. (1995)
Erf68 Salinity stress Steffens (2014)
Increasing Rice Grain Yield Under Abiotic Stresses: Mutagenesis, Genomics and... 765

salinity tolerances to other crops. They concluded that salt tolerance may be
attributed sodium dilution and compartmentalisation and build-up of osmoprotectant
compounds (De Leon et al. 2017). Similarly, molecular dissection of SST by means
of a high-density rice genetic map was constructed using a cross between varieties
Bengal and Pokkali that resulted into the development of 187 recombinant inbred
lines (RILs). These RILs were evaluated for several morpho-physiological and
biochemical characters associated with salt tolerance and were also genotyped
with 9303 SNP markers. The study leads to the identification of 85 QTLs that govern
several traits, viz. shoot Na+and K+ concentration, shoot Na+/K+ content, shoot
length/root length, salt injury score, chlorophyll content and dry weight of shoots.
Hence, construction of genetic linkage map provides new clues in understanding the
mechanism of salinity tolerance and identification of novel genes that govern salt
tolerance (De Leon et al. 2016). Cheng et al. (2012) reported isolation of salt-tolerant
QTLs by employing two sets of reciprocal IL derived from a cross between
Xiushui09 and IR2061–520–6-9 with former being salt-resistant and latter salt-
sensitive rice variety. A total of 26 QTLs linked with salt toxicity symptoms (SST)
and days to seedling survival (DSS) were identified and can be used to further
improve the salt tolerance. Gregorio et al. (2002) were successful in isolating Saltol
QTL that confers salinity stress tolerance in Pokkali by improving Na
+
/K
+
homeo-
stasis. This QTL can be intergressed into salt-sensitive varieties through marker-
assisted backcross breeding and will equip the plant breeders to create salinity-
tolerant version of otherwise high yielding rice varieties (Singh et al. 2018;
Valarmathi et al. 2019).
Drought causes substantial reduction in the overall yield of rice crops and hence is
considered main obstacle in achieving the desired goals of rice production. Hence,
plant breeding programmes are required to plan with the main aim of developing
drought tolerance in crops (Venuprasad et al. 2007). The isolation of QTLs that
govern drought tolerance plants could be useful to enhance the survival of rice
seedlings exposed to drought stress (Prince et al. 2015). Hence, MAB research is
being carried out to have a broader understanding of mechanisms of drought
tolerance and to quicken the progress of developing varieties with improved drought
tolerance (Dixit et al. 2017a,bMuthu et al. 2020). For instance, root length and
density (RLD) play an important role in mitigation of adverse effects of drought
stress, and hence indirect selection for drought tolerance through RLD is an
emerging research area in stress studies. Due to severe drawbacks in traditional
breeding, selection for RLD is cumbersome, time-consuming and laborious; hence,
advanced breeding approaches such as MAB may prove effective in improving the
drought tolerance (Siddique et al. 2015). With the advent of molecular marker
techniques, a very minute details and a broader understanding of genetics involved
in tolerance against drought in several crops including rice became available in data
repositories. A global collaboration between stress-oriented research institutes such
as IRRI, Philippines, initiated with the aim of mapping of drought-responsive QTLs
in rice (Kumar et al. 2007; Bernier et al. 2007; Venuprasad et al. 2009; Vikram et al.
2011; Dixit et al. 2014a,b). Some of the noteworthy QTLs, viz. qDTY
1.1
and
qDTY
2.1
, from the drought-resistant genotype, Apo, have been identified and are
766 A. Raina et al.

suitable for improving the drought tolerance in drought-sensitive genotypes (Muthu
et al. 2020). Recently, Uga et al. (2011) identified a key QTL (RDR Dro1) in rice on
chromosome 9 that governs deep rooting/root growth angles, thereby playing a role
in making water available under severe drought. Shamsudin et al. (2016) carried out
MAS in Malaysian rice cultivar MR219 that leads to the identification of three
drought yield QTLs, qDTY2.2, qDTY3.1 and qDTY12.1.
The QTL mapping strategy has been employed to unfold the complex genetic
control of heat tolerance in rice which is also counted as one of the main stresses that
limit the rice production to a great extent (Poli et al. 2013). In order to overcome the
deleterious effects of continuous rise in atmospheric temperature, it is imperative to
create rice varieties with improved heat tolerance (Chang-lan et al. 2005). Rice
plants usually face the negative effects of high temperature at the reproductive
stage, and hence it is very important to identify QTLs that are responsive to heat
stress at this stage. The main effects include anomalous pollination, increased pollen
sterility, reduced seed set and lower yield. Hence, the progress in breeding for heat
resistance can be rapid by detection of QTLs and candidate genes governing heat
stress tolerance at reproductive stage (Qingquan et al. 2008). A cross was made
between IAPAR-9 (heat susceptible) and Liaoyan241 (heat resistant) that leads to
the creation of RIL mapping population and identification of heat-stable QTLs
viz., qNS1, qNS4, qNS6, qRRS1, qHTS4 and qRRS4 (Li et al. 2018). Similarly,
two QTLs qPF4 and qPF6 were shown to affect the pollen fertility under high
temperature (Xiao et al. 2011). Ye et al. (2015) identified heat tolerance QTL, viz.
qHTSF1.2, qHTSF2.1, qHTSF3.1 and qHTSF4.1, at the reproductive stage in rice.
Zhao et al. (2016) while investigating the key components of molecular mechanism
for heat stress tolerance at flowering stage were successful in identifying 11 QTLs
that are linked with spikelet fertility, flowering and pollen maturation timing. Among
several QTLs, qPSLht4.1 was shown to control pollen attributes and is useful to
improve the pollen maturation and pollen tube growth. Shanmugavadivel et al.
(2017) investigated the mapping of heat tolerance QTLs and developed 272 recom-
binant inbred lines in the F8generation by crossing Nagina22 (heat resistant) and
IR64 (heat susceptible) rice varieties. This experimentation has resulted in the
identification of two QTLs qSTIPSS9.1 and qSTIY5.1/qSSIY5.1 associated with
heat tolerance at reproductive stage.
3 Conclusion
Overall, the modern biotechnological tools such as mutagenesis, transgenics and
genomics have led to the identification, cloning and characterisation of genes (from
different organisms), followed by its insertion into the rice plants with the aim of
decreasing the yield loss incurred by the different abiotic stresses. Such approaches
have brought landmark achievements by developing varieties with improved toler-
ance to various abiotic stresses.
Increasing Rice Grain Yield Under Abiotic Stresses: Mutagenesis, Genomics and... 767

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