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Chapter 8

Molecular Breeding to Improve Plant

Resistance to Abiotic Stresses

Gundimeda J.N. Rao, Janga N. Reddy, Mukund Variar,

and Anumalla Mahender

Abstract Tolerance to abiotic stress is an important agronomic trait in crops and is

controlled by many genes/quantitative trait loci (QTLs). As abiotic stresses signifi-
cantly affect grain yield, it is necessary to combat these stresses to minimize yield
losses. The current status of the study of abiotic stress tolerance suggests the general
role of some regulatory factors in the environmental adaptation mechanisms; there-
fore, it is also possible to find some common QTLs/genes influencing more than one
type of stress at a time. Identification of these factors will not only contribute to the
understanding of plant biology but also to achieve stable crop production around the
world through breeding approaches. Recent functional genomics technologies have
become the most useful tool for the understanding of tolerance to various abiotic
stresses and the genetic enhancement of various crops is being carried out by
through transfer of QTLs/genes using different approaches like marker assisted
selection (MAS) genetic engineering. In view of the impressive progress in these
areas in recent years, integration of biotechnological approaches like molecular
breeding with conventional breeding should be the major emphasis to hasten the
development of crops that are more tolerant to different abiotic stresses.

Keywords Abiotic stress • Abscisic acid • Cold • Drought • Ethylene • Freezing •

Genetic engineering • Marker Assisted Selection (MAS) • Quantitative trait loci
(QTLs) • Salinity

G.J.N. Rao (*) • J.N. Reddy • A. Mahender

Division of Crop Improvement, Central Rice Research Institute, Cuttack 753006, Odisha,
e-mail: gjnrao@gmail.com; jnreddycrri@gmail.com; mahenderbio@gmail.com
M. Variar
Central Rainfed Upland Rice Research Station, Hazaribagh 82530, India
e-mail: mukund.variar@gmail.com

© Springer International Publishing Switzerland 2016 283

J.M. Al-Khayri et al. (eds.), Advances in Plant Breeding Strategies: Agronomic,
Abiotic and Biotic Stress Traits, DOI 10.1007/978-3-319-22518-0_8
284 G.J.N. Rao et al.

8.1 Introduction

The world’s food supply is obtained either directly or indirectly from plants, but
fewer than 100 are used for food and about 50 species are actively cultivated (Burger
1981). The majority of crops such as wheat, barley, oats, rye, rice, maize, sorghum
and millet provide 56 % of the food energy and 50 % of the protein consumed on
earth (Stoskopf 1985). Cereals are the most important food crops and they continue
to be the most important source of total food consumption in the developing coun-
tries (FAO 2006); the top three cereals are maize, rice and wheat and together they
represent about 90 % of all cereals produced (http://faostat.fao.org/).
The global cereal production forecast of 2014 is nearly 2,480 million mt, down
1.4 % from 2013. While wheat production in 2014 is forecast at nearly 703 million
mt, world rice production is predicted to reach about 503 million mt (milled basis)
(FAO 2014) (http://www.fao.org/worldfoodsituation/csdb/en/). It has been esti-
mated that land degradation, urban expansion and conversion of crops and crop-
lands for non-food production will reduce the total global cropping area by 8–20 %
by 2050 (Nellemann et al. 2009). Because over 80 % of total agriculture is rainfed,
and water is vital to plant growth, any variation of precipitation patterns will have a
significant impact on agriculture, and drought is a major environmental stress reduc-
ing crop yield around the world (Bruce et al. 2002). These facts pose a formidable
challenge to increase food production by 50 % to meet the projected demand of the
world’s population by 2050.
Abiotic stresses such as drought, salinity, flood, high temperature and cold sig-
nificantly constrain plant growth and metabolism that ultimately disturbs plant
mechanism and reduces crop yield (Ahmad and Prasad 2012; Bray et al. 2000).
Crop productivity is greatly affected by abiotic stress and a 50–70 % decline in
major cereal crop production has been attributed to abiotic stresses (Mittler 2006).
For example in rice, drought stress is the largest constraint to production in rainfed
systems. In Asia, it affects 10 million ha of upland rice and over 13 million ha of
rainfed lowland rice (Pandey and Bhandari 2007); the average yield reduction in
rainfed, drought-prone areas has been found to be 17–40 % in severe drought years
(Greenbio 2011). Rice is considered to be moderately sensitive to salinity (Gregorio
et al. 1997) and soil salinity limits rice plant growth and development, resulting in
yield losses of more than 50 % (Zeng and Shannon 2000); rice yields are reduced
by 12 % for every unit of salinity (dS/ml) (Hanson et al. 1999; Maas and Grattan
1999). Flooding is a significant problem for rice farming and affects about 10–15
million ha of lowland rice fields in South and Southeast Asia and is causing an esti-
mated USD 1 billion in yield losses per year. These losses could increase consider-
ably given predicted sea level rise, as well as an increase in the frequency and
intensity of flooding caused by extreme weather events (Bates et al. 2008). Higher
growing season temperatures can significantly impact agricultural productivity,
farm incomes and food security (Battisti and Naylor 2009). Similar trends in other
cereals also suggest drastic reductions in both production and productivity due to
abiotic stresses.
8 Molecular Breeding to Improve Plant Resistance to Abiotic Stresses 285

One of the most serious long-term challenges to achieve sustainable growth in

cereal production is climate change (Adams et al. 1998; IFPRI 2001; Vaghefi et al.
2001; Wassmann and Dobermann 2007). Existing studies show that climate is the
single most important determinant of agricultural productivity, basically through
its effects on temperature and water regimes (Lal et al. 2005; Oram 1989). It is
expected that by 2100, the earth’s mean surface temperature is predicted to rise
1.4–5.8 °C and extreme events, such as floods, droughts and cyclones, are likely to
become more frequent (IPCC 2007); droughts and floods are already causing wide-
spread rice yield losses around the globe (IFAD 2009; IRRI 2010; Pandey and
Bhandari 2007). In delta and coastal regions, climate change is expected to raise
sea levels, and this will increase the risk of flooding and salinity problems in major
rice-growing areas (Mackill et al. 2010; Wassmann et al. 2004). Rice yields will be
severely affected by the increase in temperature of the earth due to the atmospheric
concentration of carbon dioxide (Peng et al. 2004). Rice yield is found to be more
sensitive to nighttime temperature: each 1 °C increase in nighttime temperature
leads to a decline of about 10 % in rice yield (Peng et al. 2004; Welch et al. 2010).
These predicted changes in climate are likely to further increase the economic
vulnerability of poor rice producers, particularly in South Asia, where more than
30 % of the population is extremely poor (with income of less than USD 1.25 per
day). Climate change presents an additional burden on the world’s agricultural and
natural resources, which are already coping with the growing food demand driven
by population growth and higher income in developing countries (Wassmann et al.
This review explores the problems and recent developments in the area of mod-
ern biology in major cereals and the future impact on production. In this chapter, the
abiotic stresses involved in major cereal crops, the advances made in the identifica-
tion of genes/QTLs associated with abiotic stresses in each crop, the breeding
attempts employing the marker-assisted approach and the results obtained are

8.2 Rice

Rice, the world’s most important cereal crop; it is the primary source of food and
calories for about one-half the world population (Khush 2005). Rice plant growth
and productivity is constantly exposed to a wide range of environmental stresses
such as drought, salinity, extreme temperatures (heat and freezing) and submergence-
reduced productivity, leading to significant crop losses globally (Bray et al. 2000).
Exhibition of a distinct or a combination of intrinsic changes ascertains the capacity
of a plant to sustain itself under unfavorable environmental conditions (Farooq et al.
2009); modified conditions in many metabolic, physiological and molecular path-
ways in plant growth can lead to serious yield losses (Bray et al. 2000; Kaplan et al.
2004; Sabehat et al. 1998; Sakamoto et al. 2004). Tolerance or susceptibility to
these abiotic stresses is a very complex phenomenon, both because stress may occur
286 G.J.N. Rao et al.

Fig. 8.1 A schematic representation of abiotic stress mechanisms and involvement of signal per-
ception and transduction pathways in cereal crops (Source: Modified from Xiong et al. 2002)

at multiple stages of plant development and more than one type of stress simultane-
ously affects the plant. Therefore, the perception of abiotic stresses and signal trans-
duction to switch on adaptive responses are critical steps in determining the survival
and reproduction of plants exposed to adverse environments (Chinnusamy et al.
2004) (Fig. 8.1).
The affect of stresses on the rice plant can be divided into biotic and abiotic
stresses, and they can be defined as any external factor exerting a negative impact
upon the plant development (Taiz and Zeiger 1998). The rice plant responds to these
environmental challenges through a number of defense mechanisms to maintain the
optimal conditions; these involve changes at the whole plant, tissue, cellular, physi-
ological and molecular levels for growth and development.
The availability of a rice genome sequence has lead to the identification of thou-
sands of molecular markers, making map-based cloning a viable option for studies
on functional genomics of rice (Jander et al. 2002). The genetic dissection of quan-
titative traits controlling the adaptive responses to abiotic stresses is a prerequisite
to allow cost-effective applications of genomics-based approaches to breeding pro-
grams (Collins et al. 2008). In this context, QTL mapping is a powerful approach
for locating genomic regions controlling complex traits (Gyenis et al. 2007). By
linking phenotypic and genotypic data, QTL mapping enables the identification of
the action, interaction, numbers and chromosomal locations of loci affecting par-
ticular traits (Miles and Wayne 2008) (Fig. 8.2).
8 Molecular Breeding to Improve Plant Resistance to Abiotic Stresses 287

Fig. 8.2 A schematic diagram illustrating the approach for development of abiotic stress tolerance

The QTL mapping approach has been employed to dissect QTLs controlling the
highly complex traits in the abiotic stress environment (Ren et al. 2005; Salvi and
Tuberosa 2005; Zheng et al. 2003). QTLs have been detected in rice for many traits
related to abiotic stress tolerance, including (a) drought (Chen et al. 2008a; Courtois
et al. 2003; Lafitte et al. 2002; Liu et al. 2009; Price et al. 2002; Shunwu et al. 2012;
Swamy et al. 2011); (b) low temperature (Baum et al. 2003; Francia et al. 2004;
Jena et al. 2010; Lou et al. 2007; Reinheimer et al. 2004; Zeng et al. 2009); (c) salin-
ity (Ammar et al. 2004; Islam et al. 2011; Sabouri and Sabouri 2008; Thomson et al.
2010); (d) submergence (Angaji et al. 2009; Neeraja et al. 2007; Septiningsih et al.
2012) and (e) heat tolerance (Cao et al. 2003; Chen et al. 2008b; Ye et al. 2012;
Zhang et al. 2008). The QTLs associated with abiotic stress tolerance in cereals are
given in Table 8.1.

8.2.1 Drought

Drought, salinity and other abiotic stresses are major causes of crop loss and this
pattern is expected to increase worldwide due to global warming, leading to a loss
of agriculturally-available land and reduced yields (Cominelli and Tonelli 2010).
An increasing amount of research is being focused on developing crops that are
resistant to abiotic stresses, such as drought, salinity, heat, cold, flooding, and

Table 8.1 QTLs associated with abiotic stress tolerance in cereals

Abiotic stress Mapping population Type Trait Crop Chr QTL LOD References
Submergence IR74/Jalmagna RILs Initial plant height Rice 1 QPh1a 10.1 Sripongpangkul et al.
Submergence IR74/Jalmagna RILs Internode increment Rice 1 QIne1 7.0 Sripongpangkul et al.
Drought CT9993-5-10-1-M/ DH Cell membrane stability Rice 8 qtl_8.2 5.6 Tripathy et al. (2000)
Submergence IR74/Jalmagna RILs Initial plant height Rice 1 QPh1a 10.1 Sripongpangkul et al.
Submergence IR74/Jalmagna RILs Internode increment Rice 1 QIne1 7.0 Sripongpangkul et al.
Submergence FR13A/CT624 DH 21 days of seedling Rice 9 Qtl.9 5.4 Kamolsukyunyong et al.
Cold Nipponbare/Kasalath RILs Germination at 15 °C Rice 4 qLTG 7.5 Miura et al. (2001)
Drought CT9993/IR62266 DH Osmotic adjustment Rice 3 Osqtl 3.1 Zhang et al. (2001)
Drought Bala/Azucena F6 Root-shoot ratio Rice 1 Phqtl 4.6 Price et al. (2002)
Drought CT9993/IR62266 DH Deep root mass Rice 1 Drqtl 3.52 Kamoshita et al. (2002)
Submergence IR49830/CT6241 DH Highly survival Rice 1 qtl.1 5.4 Toojinda et al. (2003)
Submergence FR13A/CT6241 RILs Highly survival Rice 9 qtl.9 65.8 Toojinda et al. (2003)
Drought IAC165/Co39 RILs Root thickness Rice 1 Rtqtl 3.2 Courtois et al. (2003)
Submergence IR49830/CT6241 DH High tolerance Rice 5 qtl.5 12.3 Toojinda et al. (2003)
Submergence IR49830/CT6241 F2-F3 Fast elongation Rice 9 qtl.9 16.2 Toojinda et al. (2003)
Drought Zhenshan97B/IR AT109 RILs Dry-weight of grains Rice 2 Dwqtl 2.5 Liu et al. (2006)
Heat 996/4628 F2-F3 Flowering stage Rice 4 qHsf 5.6 Govindaraj et al. (2005)
Drought Zhenshan97B/IR AT109 RILs Relative yield per plant Rice 8 QRy8 3.4 Yue et al. (2006)
Drought Zhenshan97B/IR AT109 RILs Relative spikelet fertility Rice 9 QRsf9 5.2 Yue et al. (2006)
G.J.N. Rao et al.
Drought Zhenshan97B/IR AT109 RILs Relative rate of fertile Rice 12 QRfp12 4.2 Yue et al. 2006
Drought Zhenshan97B/IR AT109 RILs Relative grain weight Rice 5 QRgw5 3.2 Yue et al. (2006)
Drought Zhenshan97B/IR AT109 RILs Relative rate of fertile Rice 12 QRfp12 4.2 Yue et al. 2006
Drought Zhenshan97B/IR AT109 RILs Relative grain weight Rice 5 QRgw5 3.2 Yue et al. (2006)
Drought Zhenshan97B/IR AT109 RILs Relative yield per plant Rice 8 QRy8 3.4 Yue et al. (2006)
Drought Zhenshan97B/IR AT109 RILs Relative spikelet fertility Rice 9 QRsf9 5.2 Yue et al. (2006)
Submergence IR49830-7/Swarna BC1F1 14 days submergence Rice 9 qtl.9 6.75 Neeraja et al. (2007)
Cold AAV002863/ DH Seedling stage Rice 1 qCtb1-a 6.33 Lou et al. (2007)
Cold AAV002863/ DH Seedling stage Rice 8 qCTS 5.91 Lou et al. (2007)
Heat Zhongyouzao8/ZYZ8 RILs Flowering stage Rice 3 qHt3 7.1 Chen et al. (2008b)
Submergence Khaiyan/IR64 BC2F1 Anaerobic germination Rice 12 qAG-12 5.71 Angaji et al. (2009)
Salinity Tarommahalli/Khazar F2 Na+ uptake Rice 1 qNAUP-1a 21.65 Sabouri and Sabouri (2008)
Heat 996/4628 F2–F3 Flowering stage Rice 2 qhts-2 2.7 Chen et al. (2008)
Submergence Khaiyan/IR64 BC2F1 Anaerobic germination Rice 1 qAG-1 4.2 Angaji et al. (2009)
Salinity Tarommahalli/Khazar F2 Seedling stage- Rice 3 qCHLC-3 20.35 Sabouri and Sabouri (2008)
chlorophyll content
Heat 996/4628 RILs Flowering stage Rice 5 qhts-5 4.6 Zhang et al. (2008)
8 Molecular Breeding to Improve Plant Resistance to Abiotic Stresses

Salinity Tarommahalli/Khazar F2 K+ uptake Rice 3 qKUP-3 19.53 Sabouri and Sabouri (2008)
Salinity Tarommahalli/Khazar F2 Fresh weight shoot Rice 1 qFWSH-1 14.45 Sabouri and Sabouri (2008)
Cold Asominor/IR24 RILs Survival rate after 7 days Rice 1 qCST 5.6 Jiang et al. (2008)
at 6 °C
Submergence Khaiyan/IR64 BC2F1 Anaerobic germination Rice 11 qAG-11 3.92 Angaji et al. (2009)
Cold Towada/MXBG BC3F5 Young panicles to the Rice 6 qCTB4-3 4.60 Zeng et al. (2009)
milky mature stage

Table 8.1 (continued)

Abiotic stress Mapping population Type Trait Crop Chr QTL LOD References
Salinity CSR27/MI48 F2-F3 Reproductive stage in leaf Rice 2 qClLR 7.57 Ammar et al. (2004)
Cold Towada/KMXBG BC3F5 Young panicles to the Rice 3 qCTB4-3 5.23 Zeng et al. (2009)
milky mature stage
Salinity CSR27/MI48 F2-F3 Seedling stage in leafs Rice 8 qNaLV 4.78 Ammar et al. (2004)
Heat Bala/Azucena RILs Relative spikelet fertility Rice 4 qtl_4 4.3 Jagadish et al. (2010)
Salinity IR29/Pokkali RILs SES tolerance score Rice 4 qSES4 3.4 Thomson et al. (2010)
Cold Norin-PL8/Kirara397 F2-F3 Anther length Rice 4 qCtb-1 8.2 Saito et al. (2010)
Salinity IR29/Pokkali BC3F5 Shoot Na+ concentration Rice 1 qSNC1 3.6 Thomson et al. (2010)
Salinity IR29/Pokkali BC3F5 Shoot Na-K ratio Rice 1 qSNK1 7.6 Thomson et al. (2010)
Cold IR66160-121-4-2-2/ RILs Spikelet fertility Rice 9 qPSST 5.4 Jena et al. (2010)
Heat Bala/Azucena RILs Spikelet fertility Rice 1 qtl_1. 6.2 Jagadish et al. (2010)
Cold IR66160-121-4-2-2/ RILs Days to heading Rice 7 qPSST- 3.6 Jena et al. (2010)
Salinity IR29/Pokkali BC3F5 Leaf chlorophyll content Rice 2 qCHL2 11.2 Thomson et al. (2010)
Cold IR66160-121-4-2-2/ RILs Culm length Rice 3 qPSST 4.2 Jena et al. (2010)
Salinity IR29/Pokkali RILs Initial SES tolerance Rice 3 qSES3 3.8 Thomson et al. (2010)
Heat Bala/Azucena RILs Leaf rolling Rice 1 qtl_1. 4.8 Jagadish et al. (2010)
Salinity IR29/Pokkali RILs Seedling survival Rice 1 qSUR1 3.2 Thomson et al. (2010)
Heat Bala/Azucena RILs Grain yield Rice 8 qtl_1. 5.6 Jagadish et al. (2010)
Salinity IR29/Pokkali RILs Seedling height Rice 2 qPH2 11.1 Thomson et al. (2010)
Drought N22/Swarna F2 Harvest index Rice 1 qDTHI1.1 18.5 Swamy et al. (2011)
Salinity BRRI dhan40/ F2-F3 Seedling staged rice Rice 8 SalTol8 7.01 Islam et al. (2011)
G.J.N. Rao et al.
Salinity BRRI dhan40/ F2-F3 Seedling staged rice Rice 1 SalTol1 2.75 Islam et al. (2011)
Drought N22/Swarna F2 Grain yield Rice 1 qDTY1.1 13.4 Swamyet al. (2011)
Salinity BRRI dhan40/ F2-F3 Seedling staged rice Rice 10 SalTol10 4.52 Islam et al. (2011)
Drought N22/IR64 F2 Date of flowering Rice 1 qDTF1.1 7.6 Swamy et al. (2011)
Drought N22/MTU1010 F2 Biomass yield Rice 10 qDTF10.1 11.8 Swamy et al. (2011)
Heat IR64/N22 BC2F1 Flowering stage Rice 1 qHD3.1 5.4 Ye et al. (2012)
Submergence R72/Madabaru F2 14 days submergence Rice 2 qSUB2.1 3.8 Septiningsih et al. (2012)
Heat IR64/N22 F2-F3 Panicle length Rice 9 qPL9.1 4.02 Ye et al. (2012)
Heat IR64/N22 BC2F1 Flag leaf length Rice 1 qFLL1.1 8.55 Ye et al. (2012)
Submergence R72/Madabaru F2 14 days submergence Rice 1 qSUB1.1 9.4 Septiningsih et al. (2012)
Submergence R72/Madabaru F2 14 days submergence Rice 9 qSUB9.1 3.6 Septiningsih et al. (2012)
Heat IR64/N22 BC2F1 spikelet fertility Rice 3 qHD1.1 6.76 Ye et al. (2012)
Submergence R72/Madabaru F2 14 days submergence Rice 12 qSUB12.1 4.2 Septiningsih et al. (2012)
Heat N22/IR64 BC2F2 Plant height Rice 1 qPH1.1 42.43 Ye et al. (2012)
Heat N22/IR64 BC2F2 Spikelet number Rice 1 qPH1.1 6.01 Ye et al. (2012)
Heat N22/IR64 F2 Spikelet fertility Rice 4 qHTSF4.1 6.66 Ye et al. (2012)
Heat N22/IR64 BC2F2 Heading date Rice 3 qHD3.1 4.24 Ye et al. (2012)
Submergence Forno/Oberkulmer RILs Germination under Wheat 4B qtl.4 3.6 Burgos et al. (2001)
8 Molecular Breeding to Improve Plant Resistance to Abiotic Stresses

Submergence Forno/Oberkulmer RILs Germination under Wheat 6A qtl.6 3.0 Burgos et al. (2001)
Submergence Forno/Oberkulmer RILs Germination under Wheat 2A qtl.2 4.2 Burgos et al. (2001)
Drought Dharwar Dry/Sitta RILs Grain yield Wheat 3 grqtl.3 5.74 Kirigwi et al. (2007)
Drought Dharwar Dry/Sitta RILs Biomass Wheat 3 grqtl.3 9.70 Kirigwi et al. (2007)

Table 8.1 (continued)

Abiotic stress Mapping population Type Trait Crop Chr QTL LOD References
Drought Hanxuan 103/Lumai 14 DH Flowering stage Wheat 4A qSwscf.1 10.26 Yang et al. (2009)
Drought Hanxuan 103/Lumai 14 DH Grain-filling Wheat 6A qSwscg 5.29 Yang et al. (2009)
Drought Hanxuan 103/Lumai 14 DH Thousand-grain weight Wheat 6B qReswc 4.18 Yang et al. (2009)
Salinity Berkut/Krichauff DH Sodium exclusion Wheat 6A qtl.6 3.8 Genc et al. (2010)
Drought C306/HUW206 RILs Physiological traits Wheat 3A qtl.3 3.5 Kumar et al. (2012)
Drought C306/HUW206 RILs Physiological traits Wheat 4B qtl.4 3.2 Kumar et al. (2012)
Cold M808/CS RILs Germination stage Wheat 5A WCBF2 5.86 Motomura et al. (2013)
Cold M808/CS RILs 7 days of old seedling Wheat 5A Wlt10 3.03 Motomura et al. (2013)
Cold M808 / CS RILs Germination stage Wheat 4B Wcor14 Motomura et al. (2013)
Cold Nure/Tremois DH Winter survival (field) Barley 5H qtl.5 6.7 Francia et al. (2004)
Cold Nure/Tremois DH Frost tolerance Barley 5H qtl.5 9.2 Francia et al. (2004)
Cold Nure/Tremois DH COR14b accumulation Barley 6H qtl.6 3.2 Francia et al. (2004)
Drought Yerong/Franklin DH Grains per spike Barley 2H GSw2.1 5.63 Xue et al. (2010)
Drought Yerong/Franklin DH Plant height Barley 6H PHw2.1 5.52 Xue et al. (2010)
Drought Yerong/Franklin DH Grain yield Barley 7H GYw1.2 7.45 Xue et al. (2010)
Drought Yerong/Franklin DH Spikes per plant Barley 7H SPw1.1 3.31 Xue et al. (2010)
Salinity Steptoe/Morex DH Ion homeostasis Barley 2H qtl.2 5.2 Nguyen et al. (2013)
Salinity Steptoe/Morex DH Shoot K+ Barley 7H qtl.7 6.81 Nguyen et al. (2013)
Salinity Steptoe/Morex DH Root dry weight Barley 3H qtl.3 5.71 Nguyen et al. (2013)
Submergence B64/teosinte F2-F3 Root aerenchyma Maize 1 RAqtl 3.0 Mano et al. (2007)
Submergence B64/teosinte F2-F3 Root aerenchyma Maize 5 RAqtl 3.6 Mano et al. (2007)
Drought and Zong3/87-1 RILs Shoot fresh weight Maize 1 qRSFW1 3.5 Liu et al. (2011)
G.J.N. Rao et al.
Drought and Zong3/87 RILs Shoot dry weight Maize 2 qRSDW2 3.1 Liu et al. (2011)
Drought and Zong3/87 RILs Leaf tolerance Maize 9 qLTD9-1 4.6 Liu et al. (2011)
Drought and Zong3/87 RILs Leaf tolerance Maize qLTD10 3.6 Liu et al. (2011)
Drought CML444/MALAW1 RILs Grain yield Maize 1 qtl1.1 7.35 Gustavo et al. (2013)
Drought CML444/MALAW1 RILs Anthesis-silking Maize 2 qtl1.2 5.34 Gustavo et al. (2013)
Drought CML440/CML504 F2-F3 Anthesis-silking Maize 6 qtl1.6 4.37 Gustavo et al. (2013)
Drought CML440/CML504 F2-F3 Grain yield Maize 3 qtl1.3 11.19 Gustavo et al. (2013)
Drought CML440/CML504 F2-F3 Grain yield Maize 3 qtl1.3 3.18 Gustavo et al. (2013)
Drought HZ32/K12 F2-F3 Physiological traits Maize 4 ph4-1 3.91 Khalid et al. (2013)
Drought HZ32/K12 F2-F3 Physiological traits Maize 6 ph6-1 3.97 Khalid et al. (2013)
Drought HZ32/K12 F2-F3 Physiological traits Maize 6 tdw6-1 4.21 Khalid et al. (2013)
Drought HZ32/K12 F2-F3 Physiological traits Maize 7 tdw7-2 5.91 Khalid et al. (2013)
Cold Shan Qui Red/SRN39 RILs germination and seedling Sorghum 2 qtl.2 4.2 Knoll et al. (2008)
Drought H77/833-2/PRLT2/89-33 RILs Transpiration, water use Pearl 1 qtl.1 3.7 Kholova et al. (2012)
leaf traits millet
Drought H77/833-2/PRLT2/89-33 RILs Leaf dry weight Pearl 2 qtl.2 4.5 Kholova et al. (2012)
8 Molecular Breeding to Improve Plant Resistance to Abiotic Stresses

Drought H77/833-2/PRLT2/89-33 RILs Shoot dry weight Pearl 7 qtl.7 8.6 Kholova et al. (2012)
DH Double haploid, RIL Recombinant inbred line
294 G.J.N. Rao et al.

nutrient limitation (Collins et al. 2008; Witcombe et al. 2008). Of these stresses,
drought is the most serious constraint to rice production in less favorable rice-grow-
ing areas and most of the popular farmers’ varieties are susceptible (Serraj et al.
2009). Depending on the timing and severity of drought stress at the crop develop-
mental stage, drought can be categorized into three types: vegetative, intermittent
and terminal (Chang et al. 1979; Fischer et al. 2003; Kamoshita et al. 2008). Of
these three, the occurrence of terminal drought stress at the reproductive stage dur-
ing the cropping season directly affects grain yield and has devastating conse-
quences (Fukai et al. 2001; Lanceras et al. 2004; Tsubo et al. 2006; Venuprasad
et al. 2009). The severity of drought stress levels depends on various factors such as
soil type, evaporation, transpiration rate, temperature, relative humidity and rainfall
pattern (Fischer et al. 2003). The major drawbacks for the development of drought-
tolerance cultivars include lack of effective selection criteria for drought tolerance
related traits such as morphological, physiological traits and molecular mechanisms
of genes and low heritability of grain yield under stress; these are key reasons for
the slow progress in drought tolerance in plant breeding (Ouk et al. 2006).

8.2.2 MAS Approaches in QTL and Genes

Marker assisted selection (MAS) is one of the best approaches for the development
of drought tolerance (DT) in rice, a major target for the plant breeders and biotech-
nologists (Jongdee et al. 2002). For effective implementation of MAS in a rice-
breeding program for drought tolerance, targeted QTL/gene must have a large effect
on grain yield under stress and be consistently expressed in different backgrounds.
Therefore, it is imperative to identify background-independent drought-tolerance
QTLs from rice germplasm resources and corresponding tightly-linked molecular
markers for developing DT cultivars by MAS (Fig. 8.2) (Table 8.2). However, the
successful use of QTLs in marker-assisted selection depends on their effect and
consistency across genetic backgrounds and environments. Most of the QTLs for
grain yield under drought have been mapped against a single genetic background in
early-segregating generations (F3, BC2 and BC2F2) and were evaluated in a limited
number of environments (Swamy et al. 2011).
QTL mapping has been carried out in an attempt to determine the genetic basis of
several traits related to drought tolerance, including the following: (a) deep rooting
(Ekanayake et al. 1985; Lilley and Fukai 1994; Pantuwan et al. 2002; Wade et al.
2000); (b) osmotic adjustment (Babu et al. 2003; Jongdee and Cooper 1998; Ludlow
and Muchow 1990; Robin et al. 2003; Zhang et al. 1999; Zhu et al. 1997); (c) cell
membrane stability (Tripathy et al. 2000); (d) abscisic acid (ABA) content (Quarrie
et al. 1994, 1997); (e) stomatal regulation Price and Tomos 1997; (f) leaf water status
and root morphology (Ali and Awan 2004; Champoux et al. 1995; Courtois et al.
2000; Kamoshita et al. 2002; Price and Tomos 1997; Price et al. 2002; Ray et al. 1996;
Yadav et al. 2002; Zhang et al. 2001; Zheng et al. 2000); (g) root thickness (Courtois
et al. 2003); (h) root dry weight, pulling force, and root length and ratio of shoot and
8 Molecular Breeding to Improve Plant Resistance to Abiotic Stresses 295

Table 8.2 Abiotic stress tolerance genes/transcription factors in cereal and other crops
Abiotic stress Genes/transcription
tolerance levels factor Crop References
Drought and salinity PSP 1015 Wheat Hollung et al. (1994)
Cold Tacr7 Wheat Gana et al. (1997)
Cold tolerance OscodA Rice Sakamoto and Alia
Murata (1998)
Salinity Mn-SOD Rice Tanaka et al. (1999)
Salinity OsA1/ OsA2 Rice Zhang et al. (1999)
Drought, cold and ABF4 Arabidopsis Choi et al. (2000)
salinity thaliana
Salinity and cold GS2 Rice Hoshida et al. (2000)
Cold ScRPS7 Wheat Berberich et al. (2000)
Osmotic and drought TaSAMDC Wheat Li and Chen (2000)
Cold CHT9 Wheat Yet et al. (2000)
Drought and salinity OsCDPK7 Rice Saijo et al. (2000)
Salinity OsGS2 Rice Hoshida et al. (2000)
Drought, Cold and OsCDPK7 Rice Sajjo et al. (2000)
Cold tolerance OsCtb1 Rice Saito et al. (2001)
Water logging Pdc1 Rice Rahaman et al. (2001)
Salinity and drought Osmotin Rice Barthakur et al. (2001)
Cold AtCBF2 Tomato Hsieh et al. (2002)
Drought PDH A. thaliana Mani et al. (2002)
Cold tolerance MYBS3 Rice Jang et al. (2003)
Drought and cold TaDREB1 Wheat Shen et al. (2003a)
Drought and salinity AhDREB1 Tobacco Shen et al. (2003b)
Cold OsDREB1A, Rice Dubouzet et al. (2003)
Salinity and OsDREB2A Rice Dubouzet et al. (2003)
Drought mtlD Wheat Abebe et al. (2003)
Drought betA Maize Quan et al. (2004)
Drought and salinity RD26 A. thaliana Fujita et al. (2004)
Drought and freezing NPK1 Maize Shou et al. (2004)
Salinity OsNHX1 Rice Fukuda et al. (2004)
Drought TaLTP1 Wheat Pellegrineschi et al.
Drought DREB1A Wheat Jang et al. (2004)
Drought and salinity OsRacB Rice Luo et al. (2006)
Salinity TVP1 Wheat Brini et al. (2005)
Salinity OsHKT1 Rice Kader et al. (2006)
Drought, cold and OsDREB1B Rice Ito et al. (2006)
Drought, cold and WDREB2 Wheat Egawa et al. (2006)
Salt and submergence AtMYB44 A. thaliana Yanhui et al. (2006)
296 G.J.N. Rao et al.

Table 8.2 (continued)

Abiotic stress Genes/transcription
tolerance levels factor Crop References
Cold and heat OsDREB1B Rice Qin et al. (2007)
Salinity, drought and OsDREB1F Rice Wang et al. (2008)
Drought TPS1-TPS2 Nicotiana Karim et al. (2007)
Drought and cold HvCBF4 Rice Oh et al. (2007)
Salinity AeNHX1 Wheat Qiao et al. (2007)
Drought ZmNF-YB2 Maize Nelson et al. (2007)
Drought OsDREB1G Rice Chen et al. (2008)
Drought and cold Wlip19 Wheat Kobayashi et al. (2008)
Drought and salinity OsAB15 Rice Zou et al. (2008)
Drought and salinity OsbZIP23 Rice Xiang et al. (2008)
Drought CodA Solanum Ahmad et al. (2008)
Drought Rab16D Rice Zou et al. (2008)
Cold tolerance HOS10 Rice Chen et al. (2008)
Drought TsVP Maize Li et al. (2008)
Cold GmWRKY21 A. thaliana Zou et al. (2008)
Salinity OsWRKY45-2 Rice Tao et al. (2009)
Drought Os AP59 /Os AP37 Rice Oh et al. (2009)
Drought, heat and ZmbZIP17 Maize Jia et al. (2009)
Salinity CaZF Tobacco Jain et al. (2009)
Drought and salinity ONAC045 Rice Zheng et al. (2009)
Salinity and drought OsDHODH1 Rice Liu WY et al. (2009)
Submergence SNORKEL1/ Rice Hattori et al. (2009)
Drought Dro1 Rice Uga et al. (2011)
Drought, cold and OsABF2 Rice Hossain et al. (2010)
Salinity and cold TaSnRK Wheat Zhang et al. (2010)
Drought cold and OsDREB1 Rice Fukao et al. (2011)
Hyperosmotic PgDREB2A Tobacco Agarwal et al. (2010)
Drought OsNAC10 Rice Jeong et al. (2010)
Cold Osmyb4 Rice Park et al. (2010)
Drought and salinity OsAREB1 Rice Jin et al. (2010)
Drought Oshrf1 Rice Zhang et al. (2011)
Drought and cold SbDREB2 Sorghum Bihani et al. (2011)
Drought and salinity OSRIP18 Rice Jiang et al. (2012)
Drought and OsERF3 Rice Wan et al. (2011)
8 Molecular Breeding to Improve Plant Resistance to Abiotic Stresses 297

Table 8.2 (continued)

Abiotic stress Genes/transcription
tolerance levels factor Crop References
Drought SbDREB2 Sorghum Bihani et al. (2011)
Drought and salinity OsRIP18 Rice Jiang et al. (2012)
Drought OsGRF8 Rice Choi et al. (2004)
Osmotic tolerance OsGRF8 Rice Choi et al. (2004)
Drought and salinity OsHsfA7 Rice Liu et al. (2013)
Cold Wlt10 Wheat Motomura et al. (2013)
Cold Wdhn13 Wheat Motomura et al. (2013)
Cold Wcor14 Wheat Motomura et al. (2013)

root (Champoux et al. 1995; Nguyen et al. 2004; Price et al. 2002; Robin et al. 2003;
Uga et al. 2011; Zhang et al. 2001; Zheng et al. 2000); (i) stomatal closure (Lv et al.
2007); (j) relative water content (Altinkut et al. 2001; Colom and Vazzana 2003); (k)
photosynthetic rate (Hetherington and Woodward 2003; Woodward et al. 2002); (l)
chlorophyll stability index (Ananthi and Vanangamudi 2013); (m) leaf rolling (Hsiao
1973); (n) proline accumulation (Gunes et al. 2005; Shao et al. 2005); (o) signal trans-
duction, osmoregulation and antioxidant systems (Hare et al. 1999; Kishor et al. 2005;
Szabados and Savoure 2009); (p) stomatal conductance and transpiration rate (Chaves
and Oliveira 2004; Lawlor and Cornic 2002); (q) grain yield and yield components
(Lafitte et al. 2004; Xu et al. 2005); (r) stay green (Jiang et al. 2004); (s) canopy tem-
perature, leaf rolling and leaf drying (Yue et al. 2006); (t) grain yield (Kirigwi et al.
2007; Salem et al. 2007) and (u) thousand grain weight (Nezhad et al. 2012), are all
associated to some degree with drought tolerance.
Since drought tolerance characters are quantitative in nature, the complete
genetic dissection of these complex traits into component genetic factors is a pre-
liminary task. Many drought-related QTLs have been identified in major cereal
crops that can be effectively used in breeding programs. This necessitates that more
and more replicated yield tests should be conducted in order to accurately character-
ize their effects and to evaluate their stability across different environments
(Cattivelli et al. 2008) (Table 8.1). Tolerance to High Temperature

Heat stress, especially during the flowering stage in rice, affects the seed setting rate
and floret sterility, resulting in high yield losses (Morita et al. 2005; Peng et al.
2004). In a climate-change scenario, when day temperatures are predicted to rise to
alarming levels, research on the genetic mechanisms of heat tolerance becomes
more relevant and the development of new rice varieties with heat tolerance gene(s)
are a high-priority area. The main cause of spikelet sterility induced by high tem-
perature at the flowering stage is anther indehiscence. The anthers of heat-tolerant
cultivars dehisce more easily than those of susceptible cultivars under high tempera-
ture conditions (Mackill et al. 1982; Matsui et al. 1997a, b, 2001; Satake and Hayase
298 G.J.N. Rao et al.

1970). This is because of the tight closure of the locules by the cell layers, which
delays locule opening and decreases spikelet fertility (Matsui and Omasa 2002); it
has been suggested that spikelet fertility at high temperature can be used as a screen-
ing tool for heat tolerance during the flowering stage (Prasad et al. 2006).
In recent years, with the development of molecular-marker techniques and their
widespread application, there were reports of genetic research on heat tolerance in
rice by utilizing molecular markers (Cao et al. 2003; Zhao et al. 2006). Much effort
has been made to carry out molecular mapping of heat tolerance quantitative trait
loci (QTLs) in rice at the booting, flowering and grain filling to ripening stages
(Jagadish et al. 2010; Xiao et al. 2011; Ye et al. 2012; Zhang et al. 2008) and QTL
mapping studies for heat tolerance have been conducted on various rice populations
at the booting (Zhao et al. 2006) and flowering stages (Cao et al. 2003; Chen et al.
2008; Jagadish et al. 2010; Xiao et al. 2011; Zhang et al. 2008). However, confirma-
tion and fine mapping of the identified QTL for heat tolerance have not been
reported. Using identified genetic resources and QTLs to improve heat tolerance in
rice varieties has not been achieved. Further studies on QTL mapping using accu-
rate phenotyping technology and validation of mapped major QTLs in different
populations are needed to identify candidates for map-based cloning of genes which
account for heat tolerance in rice (Table 8.1). Cold Tolerance

Chilling injury is one of the most important limiting factors affecting rice produc-
tion in temperate and high-elevation areas. Rice is sensitive to low temperature and
its growth and production is reduced dramatically at low temperature (Lou et al.
2007). Good cold tolerance at the seedling stage is an important character for stable
rice production, especially in direct-seeded fields. Development of varieties having
tolerance to cold is one of the effective ways to avoid the low temperature damage.
Low temperature often affects plant growth and productivity, which causes sig-
nificant crop yield losses (Xin and Browse 2001). Plants differ in their tolerance to
chilling (0–15 °C) and freezing (<0 °C) temperatures. In general, plants from
temperate climatic regions are considered to be chilling tolerant to a variable degree,
and can increase their freezing tolerance by being exposed to chilling, non-freezing
temperatures, a process known as cold acclimation, which is associated with bio-
chemical and physiological changes (Gilmour et al. 2000; Shinozaki and Yamaguchi-
Shinozaki 1996; Thomashow 1998) and ultimately exhibited marked changes in
gene expression, bio membrane lipid composition and small molecule accumulation
(Yamaguchi-Shinozaki and Shinozaki 2006). Conventional breeding methods have
met with limited success in improving the cold tolerant crops due to the complexity
of stress tolerance traits, low genetic variance of yield components under stress
condition and lack of efficient selection criteria. It is important, therefore, to look
for alternative strategies to develop cold stress tolerant crops.
Biotechnology offers new strategies that can be used to develop transgenic crop
plants with improved tolerance to cold stress. Molecular markers have facilitated
8 Molecular Breeding to Improve Plant Resistance to Abiotic Stresses 299

the identification of chromosomal regions associated with many complex traits in

rice including tolerance to low temperature. Identification of QTLs related to low
temperature tolerance in rice have been reported by utilizing RFLP markers
(Harushima et al. 1998; Takeuchi et al. 2001) and microsatellite markers (Andaya
and Mackill 2003; Fujino et al. 2004; Kuroki et al. 2007; Lou et al. 2007; McCouch
et al. 2002; Suh et al. 2010).
Saito et al. (1995) identified two QTLs responsible for the cold tolerance at the
booting stage which were mapped on chromosomes 3 and 4 in populations derived
from Norin/Pl8 cross combination. Fine mapping of the QTL on chromosome 4 has
identified two genes (Ctb1 and Ctb2) for cold tolerance in a 56 kb region (Saito
et al. 2001). The QTL for cold tolerance on chromosome 4 of Norin/PL8 cross com-
bination consists of two closely linked genes, related to cold tolerance and anther
length, and Ctb1 was delimited to seven open reading frames (ORFs) in a 56-kb
region (Saito et al. 2004). Several QTLs linked to cold tolerance at the reproductive
stage were mapped on different chromosomes using F2, BC5F3 and doubled-haploid
(DH) populations (Andaya and Mackill 2003; Dai et al. 2004; Liu et al. 2003; Saito
et al. 2001; Suh et al. 2010; Xu and Crouch 2008; Ye et al. 2010). A QTL for cold
tolerance between RM5647 and PLA61 on chromosome 8 explains 26.6 % of the
phenotypic variance, and its additive effect is 11.4 % (Kuroki et al. 2007). The
QTLs reported on chromosomes 1, 2, 3, 5, 6, 7, 9 and 12 explain 11–17 % of the
phenotypic variance identified to confer cold tolerance at the booting stage (Andaya
and Mackill 2003). Consequently, it is crucial to screen for cold tolerance at this
stage and to understand the genetic basis and molecular mechanisms of cold toler-
ance. Despite many QTL mapping reports on cold tolerance at the booting stage,
cold tolerance-related traits have not been studied in large populations over time and
at different locations (Table 8.1). Submergence

Submergence stress is a widespread problem in rice-growing areas, especially in the

flood-prone rainfed lowlands and it was reported that 22 million ha per year of in
South and Southeast Asia have been affected at various stages (Jackson and Ram
2003; Ram et al. 2002). Different flooding types include flooding during seed ger-
mination (anaerobic germination), flash flooding (submergence), stagnant flooding
and deeper stagnant flooding. In the field, more than one of these situations can
occur in the same season or in different seasons (Ismail et al. 2009). Plants subjected
to submergence stress are exposed to low light, limited gas diffusion, effusion of
soil nutrients, mechanical damage and increased susceptibility to pests and diseases
that ultimately affect the grain yield (Ram et al. 2002).
Submergence itself can be classified into flash flooding and deepwater flooding
according to the duration of flooding and the water depth (Bailey-Serres et al. 2010;
Jackson and Ram 2003). Flash flooding, which generally lasts only a few weeks, is
caused by heavy rain but standing water is only present for a short duration. On the
other hand, deepwater flooding, extending for several months, occurs during the
300 G.J.N. Rao et al.

rainy season, and with standing water levels reaching several meters (Hattori et al.
2011). Flooding can cover the entire plant for a prolonged period; most rice culti-
vars die within 7 days of complete submergence (Bailey-Serres et al. 2010; Xu et al.
2006). A limited number of rice cultivars overcome submergence through antitheti-
cal growth responses.
Recent studies provide insights into the hormonal control of submergence toler-
ance. According to Fukao and Bailey-Serres (2008), under submerged conditions,
the concentration of ethylene increases while the concentration of abscisic acid
(ABA) decreases. In intolerant plants, this triggers an increase in gibberellic acid
(GA) and the induction of cell elongation. In tolerant plants, the ethylene-induced
increase in SUB1A expression and inhibits the accumulation of GA by increasing
the accumulation of the GA-signaling suppressors thus decreasing the GA respon-
siveness. Under complete submergence, the presence of SUB1A in the submergence-
tolerant genotypes suppresses the perception and production of ethylene via its
induction of the Slender Rice-1 (SLR1) and SLR Like-1 (SLRL1) genes (Fukao and
Bailey-Serres 2008).
Deepwater rices responds to submergence by promoting internode elongation to
outgrow floodwater levels. This escape response is regulated by a polygenic locus
that encodes two APETALA2/ Ethylene Response Factor (AP2/ERF) DNA binding
proteins, SNORKEL 1 (SK1) and SNORKEL 2 (SK2) (Hattori et al. 2011). The
AP2/ERF super family of rice can be divided into three families based on sequence
similarity and number of domains: AP2, ERF and RAV. Of these, the ERF family is
classified into 14 groups (I–XIV) based on gene structures, phylogeny and con-
served motifs (Nakano et al. 2006).
Submergence tolerance is controlled by a single major QTL on chromosome 9,
along with a number of minor QTLs (Toojinda et al. 2003; Xu and Mackill 1996).
All studies on submergence have used the traditional genotype FR13A, which is one
of the most submergence-tolerant donor varieties. The major QTL, named Sub1,
with a LOD score of 36 and an R2 value of 69 % that provides tolerance to complete
submergence for up to 2 weeks, has been identified as a major determinant of sub-
mergence tolerance in rice variety FR13A and its derived progenies (Xu and Mackill
1996). More recently, Sub1 has been fine-mapped and cloned, yielding three candi-
date genes, Sub1A, Sub1B and Sub1C (Fukao et al. 2006; Ruanjaichon et al. 2008;
Xu et al. 2006).
Sub1A containing an ethylene-response-factor (ERF) domain, was first cloned
from rice variety FR13A (Flood Resistant 13A) (Xu et al. 2006). The ethylene-
response-factor (ERF) domain composed of a super family of transcription factors
in plants and microorganisms (Nakano et al. 2006; Okamura et al. 1997). EREBPs
are characterized by the presence of the highly-conserved EREBP DNA-binding
domain of about 60 amino acids (Okamura et al. 1997). Plant proteins that contain
ERF domains are known regulators of abiotic and biotic stress responses (Gutterson
and Reuber 2004; McGrath et al. 2005; Rahman et al. 2001). Within the sequenced
Sub1 locus of an FR13A derived tolerant breeding line, three putative ERF genes
were identified and designated SUB1A-1, SUB1B-1, and SUB1C-1 (Xu et al.
8 Molecular Breeding to Improve Plant Resistance to Abiotic Stresses 301

2006). ERF family members control diverse biological functions in growth and
development such as leaf epidermal cell density, flower development and embryo
development (Boutilier et al. 2002; Elliott et al. 1996), as well as hormonal signal-
ing mediated by ethylene, cytokinin (Rashotte et al. 2006) and brassinosteroid
(Alonso et al. 2003; Hu et al. 2004). ERFs are also involved in response to biotic and
abiotic stimuli such as pathogen infection, drought and freezing stresses (Gilmour
et al. 2000; Hao et al. 1998; Liu et al. 1999).
The SUB1A gene is absent from the Nippon bare reference genome and all other
analyzed Oryza sativa japonica varieties due to an inversion and deletion. In intol-
erant O. sativa indica varieties, the SUB1A gene is either absent or present as the
allelic variant SUB1A-2. Single nucleotide polymorphisms (SNPs) were also iden-
tified for the SUB1C gene, distinguishing the tolerant SUB1C-1 allele from those
found in intolerant varieties (SUB1C-2–SUB1C-7). In contrast, no tolerant-specific
allele for SUB1B was identified (Xu et al. 2006). Gene expression analyses showed
that all three ERF genes were induced under submergence and revealed a specifi-
cally high SUB1A and low SUB1C expression in tolerant varieties. SUB1A had
been subsequently identified as the major determinant of tolerance by a transgenic
approach showing that constitutive expression of the SUB1A-1 allele conferred tol-
erance of submergence to an intolerant variety (Liaogeng) that naturally lacks the
SUB1A gene (Xu et al. 2006).
A breakthrough in the development of submergence-tolerant varieties was facili-
tated by the fine-mapping and sequencing of the Sub1 locus (Collard and Mackill
2008; Septiningsih et al. 2009; Toojinda et al. 2003; Xu and Mackill 1996).
Accordingly, precise gene-based markers have been designated as SUB1 and used
for its successful introgression into popular rice varieties (Neeraja et al. 2007;
Septiningsih et al. 2009; Siangliw et al. 2003; Singh et al. 2009; Toojinda et al.
2003). This SUB1gene was transferred into six Asian rice mega-varieties (those
widely grown in Asia), namely: Swarna, Samba Mahsuri, IR64, BR11, Thadokkam
1 (TDK1) and CR1009. These mega-varieties, possessing agronomic and quality
traits preferred by farmers, were introgressed with the SUB1 gene using marker-
assisted backcrossing (MABC) (Mackill et al. 2006; Neeraja et al. 2007; Septiningsih
et al. 2009). When the SUB1A locus of FR13A was introgressed into the rice vari-
ety Swarna via marker-assisted selection, the resultant new variety showed enhanced
submergence tolerance.

8.3 Wheat

8.3.1 Drought

Because wheat (Triticum aestivum L.) is the cereal of choice in most countries,
constant efforts are needed to boost its production to keep pace with the ever-
increasing population. But unfortunately, these efforts are being hampered by a
302 G.J.N. Rao et al.

number of abiotic stresses among which drought is most important (Boyer 1982).
According to Pfeiffer et al. (2005), 50 % of wheat production area is affected by
drought worldwide. Drought leads to abnormal germination and poor crop stand
(Harris et al. 2002; Kaya et al. 2006). Furthermore, drought stress at various critical
growth stages like flowering and grain filling greatly reduces crop yield and for that
reason its importance has been recognized at the global level. Thus, developing
drought-resistant cultivars has been a major objectives of plant breeders and plant
Although considerable efforts have been made to develop drought-tolerant culti-
vars of wheat through conventional breeding approaches, they met with little suc-
cess due to the quantitative (polygenic) nature of drought tolerance, which is more
influenced by external environmental conditions than by the genetic component
(Ingram and Bartels 1996; Zhang 2004). The affects of drought stress on plant
growth and development have been observed to impact cells, tissue and organs
(Beck et al. 2007) and their mechanisms influence major regulations at the morpho-
logical, physiological and molecular levels (Farooq et al. 2009; Xiong et al. 2002).
Due to the increased understanding of gene structure and function at the cellular
and molecular levels (Gosal et al. 2009), genomic-based approaches can now pro-
vide excellent opportunities to search and map QTLs for drought tolerance. Previous
reports indicated that various DNA markers such as RFLP, AFLP and SSR have
been used to tag QTLs for drought stress in wheat (Quarrie et al. 2005). Kirigwi
et al. (2007) used SSR and EST markers for mapping QTL on chromosome 4A for
grain yield and yield components in wheat. The markers associated with the QTL
were XBE637912, Xwmc89, and Xwmc420. Quarrie et al. (2005) conducted map-
ping of QTLs for drought tolerance in hexaploid wheat which were located on chro-
mosomes 1A, 1B, 2A, 2B, 2D, 3D, 5A, 5B, 7A and 7B. Thus, the DNA markers
closely linked with QTLs conferring drought tolerance would greatly enhance the
selection efficiency (Cattivelli et al. 2008).

8.3.2 MAS Approaches Cold Stress

Cold/freezing temperatures represent one of the significant abiotic stresses limiting

geographical distribution of plants and reducing crop quality and productivity. Freezing
tolerance, one of these complex traits, is acquired through the cold acclimation process
in many overwintering plants of temperate regions (Thomashow 1999).
A large number of genes with various functions are induced during cold acclima-
tion (Rabbani et al. 2003; Seki et al. 2002). In particular cold-responsive (Cor)/late-
embryogenesis-abundant (Lea) genes are transcriptionally activated in cold
acclimation, and the accumulated COR/LEA proteins lead to protection of the
integrity of cell structures and functions from freezing damage (Kosova et al. 2010;
Thomashow 1999). Most Cor/Lea genes, including Wlt10, Wdhn13 and Wcor14,
show differential expression levels in two wheat cultivars with contrasting levels of
8 Molecular Breeding to Improve Plant Resistance to Abiotic Stresses 303

freezing tolerance under low temperature conditions (Kobayashi et al. 2004; Ohno
et al. 2003; Tsvetanov et al. 2000). Over-expression of the wheat CBF/DERB tran-
scription factors increases freezing tolerance of transgenic plants (Kobayashi et al.
2008; Morran et al. 2011). The CBF regulon controls one of the important regula-
tory pathways in development of freezing tolerance in wheat (Winfield et al. 2010).
In common wheat, Vrn-1 and Fr-1 are well-known major quantitative trait loci
determining the vernalization requirement for flowering and winter hardiness. The
two loci are linked on the long arms of homoeologous group 5 chromosomes (Galiba
et al. 1995; Sutka et al. 1999). The CRT/DRE, ABRE and other cold-responsive
motifs have been identified in the 5′ upstream regions of many Cor/Lea genes in
common wheat. Wcbf2 genes encode a putative transcription factor recognizing the
CRT motif (Takumi et al. 2003).
The WCBF2 cascade is tightly associated with cold acclimation and the Fr-1
alleles, whereas expression of the cold-responsive Vrn-1 candidate gene WAP1 is
apparently not related to expression of the Wcbf2 gene (Kobayashi et al. 2005).
Expression of other cold-responsive transcription factor genes, Wdreb2 and Wlip19,
are weakly controlled by Fr-1, while Wabi5 transcription factor gene involved in the
ABA-dependent pathway appears to act independently of Fr-1 (Kobayashi et al.
2004). Mutant analyses suggest that ABA sensitivity is not associated with cold
acclimation, while ABA is involved in determination of the basal level of freezing
tolerance in wheat. Thus, the CBF-mediated Cor/Lea gene expressions play central
roles in cold acclimation to develop high levels of freezing tolerance in wheat. Salinity

Salt tolerance in cereals is known to be associated with the control of shoot Na+
content; with tolerant lines having more efficient systems to exclude sodium from
their shoots. A single locus (Kna1) localized on chromosome 4D of wheat was
shown to control K+/Na+ discrimination and in a saline environment, bread wheat
(AABBDD) accumulates less Na+ and more K+ than durum wheat (AABB)
(Dubcovsky et al. 1996). Loci involved in salt tolerance have been identified on
chromosomes 4H and 5H of barley, Hordeum vulgare, and 1Hch, 4Hch and 5Hch of
H. chilense (Forster et al. 1990) thus showing that the gene pool of wild relatives
may represent an important source of new loci for salt tolerance. A number of QTLs
affecting salt tolerance were detected on 1H, 4H, 6H and 7H chromosomes.

8.4 Maize

8.4.1 Drought

Drought is one of the important abiotic stresses which results in significant yield
losses in maize (Zea mays L.). It is necessary to overcome the drought effects in
order to minimize yield losses. Although drought stress affects maize in almost all
304 G.J.N. Rao et al.

growth stages, it is extremely sensitive in the period from 1 week before to 3 weeks
after flowering (Banziger et al. 2000). Maize is widely regarded to be more suscep-
tible to drought at flowering stage than other rainfed crops. This is due to a combina-
tion of several factors including physical separation of male and female flowers,
floral asynchrony, non-receptivity of the silk, tassel blasting, trapped anthers and
embryo abortion (Lu et al. 2011). Consequently, breeding maize for reproductive-
stage drought tolerance could lead to the development of improved varieties able to
withstand varying degree of water stress (Messmer et al. 2009; Zhu et al. 2011).
Tolerance to drought in maize is a polygenic trait and typically has low heritabil-
ity and is characterized by high genotype x environment interaction (GEI). In the
genetic improvement of maize, QTL, MAS and genetic engineering approaches are
becoming the most useful tools to develop drought-resistant maize genotypes.
Conventional breeding based on direct selection of phenotypes under drought has
led to impressive yield gains in maize but underlying genetic causes largely remain
unknown. QTL-based approaches can contribute significantly to the understanding
of the genetic basis of crop performance, especially under drought-stress conditions
and such knowledge may be crucial in designing cost-effective breeding approaches
aimed at improving sustainability and stability of grain yield under adverse condi-
tions (Collins et al. 2008).

8.4.2 QTL Mapping

Drought tolerance QTL studies in maize and other crops and the strategies for their
use in MAS breeding programs have been extensively discussed in several compre-
hensive reviews (Araus et al. 2008; Collins et al. 2008; Tuberosa and Salvi 2009).
QTL mapping for grain yield (GY) underwater stress and other associated traits
such as anthesis silking interval (ASI) have been an active area of research espe-
cially in the past two decades. The QTL detected under water-stress and well-
watered (WW) conditions can be categorized according to the stability of their
effects across environmental conditions. A constitutive QTL is consistently detected
across most environments, while an adaptive QTL is detected only in specific envi-
ronment such as WS conditions (Collins et al. 2008). One of the earliest studies
involving tropical germplasm under managed stress conditions identified 13 QTLs
on chromosomes 1, 2, 4, 6, 7, 8 and 10 for grain yield, of which QTLs on chromo-
somes 1 and 10 were stable across WW and WS environments (Ribaut et al. 1997).
Since then, a number of QTL regulating morpho-physiological component traits as
well as GY have been reported in maize (Li et al. 2010; Messmer et al. 2009, 2011).
Although genetic dissection of drought tolerance in maize seems to have been
widely reported, successful practical application of identified QTLs in maize
improvement programs are scarce. The reasons are manifold, including genetic
complexity, influence of genetic background, epistasis, profound QTL x environ-
ment interactions (QEI), population-specific nature of identified QTL and involve-
ment of donor lines that are not agronomically elite (Collins et al. 2008; Truntzler
et al. 2010).
8 Molecular Breeding to Improve Plant Resistance to Abiotic Stresses 305

8.4.3 QTLs of Drought Tolerance in Wheat and Barley

Most QTLs for drought tolerance in wheat, and its close relative barley, have been
identified through yield and yield component measurements under water-limited
conditions (Maccaferri et al. 2008; Mathews et al. 2008; McIntyre et al. 2009;
Quarrie et al. 2006). Although yield is the most relevant trait to breeders, it is very
difficult to describe accurately with respect to water use and to identify candidate
regions for positional cloning. For this reason, very few studies have identified
QTLs associated with specific components of drought response. Although the
development of gene-based molecular markers and genome sequencing should
accelerate positional cloning (Collins et al. 2008), the genomic regions associated
with individual QTL are still very large and are presently unsuitable for screening
in a breeding program.
The effect of drought on reproductive processes has been extensively described
in cereals (Barnabas et al. 2008). Passioura (2007) suggested that floral infertility
resulting from water deficit could be a promising target for improvement but no
QTL studies for this trait have been published in wheat or barley. Improving the
competence of the root systems to extract water from the soil also seems an obvious
target for genetic analysis.
The identification of markers or genes associated with root growth and architec-
ture would be particularly useful for breeding programs to improve root traits by
molecular marker-assisted selection. Few papers have described work on the identi-
fication of QTLs for root traits in wheat. Ma et al. (2005) found a QTL for root
growth rate under Al treatment. QTLs of root traits (primary/lateral root length and
number, root dry matter) under control conditions and during nitrogen deficiency
were identified in wheat (Laperche et al. 2006). However, QTLs corresponding to
root architecture in dry environments are yet to be discovered in wheat and barley.
The genetic basis of drought tolerance has been studied extensively in maize and
other taxa (Ribaut and Ragot 2007; Tuberosa et al. 2002). Over the past few years
there have been several mapping studies that have targeted drought tolerance and
other abiotic stress tolerance loci associated with performance in low-yielding envi-
ronments. However, despite this substantial research effort the only markers that
have found their way into practical plant breeding programs are those for boron and
aluminium tolerance (Gupta et al. 2010).

8.5 Barley

Barley (Hordeum vulgare L.) is an important cereal crop in the Near East, Asia,
Central Africa, North and South America, and Europe. It occupies more than 40
million ha in developing countries where often it is the only possible rainfed crop
that farmers can grow (Ceccarelli 1994). It is an annual, diploid self-pollinating spe-
cies with a relatively short life cycle. Its importance derives from the ability to grow
and produce in marginal environments that are often characterized by drought and
306 G.J.N. Rao et al.

low-temperature conditions. Among the cereals, barley is considered a good genetic

model for the Triticeae tribe to study plant response to adverse environmental con-
ditions. Its inbreeding behavior and diploidy make genetic studies easy to perform.
It is a model species for genetic and physiological studies and shows a wide range
of adaptations to various habitats; its wide range of adaptability, the availability of
a wide range of genetic stocks, and the extended colinearity with other members of
the tribe are additional advantages as a model (Hayes et al. 2003).
Molecular mapping of genes controlling plant resistance to drought stress has
lagged behind that for disease resistance and morphological characters because of
the complexity of drought tolerance and its association with many traits.
Molecular markers have played an important role in understanding the genetic
basis of economically-important traits in barley. Over the last decade, comprehen-
sive genetic maps have been constructed for seven barley chromosomes and have
been used in QTL analysis (Kleinhofs and Graner 2001) and to isolate genes through
map-based cloning (Kilian et al. 1995). An important use of markers has been MAS,
which is made possible by the identification of markers linked to
commercially-important traits such as disease resistance (Graner et al. 1996),
response or tolerance to abiotic stress (Forster et al. 2000) and seed or feed quality
Several approaches have been pursued to detect sequence polymorphisms in bar-
ley relying on hybridization RFLP-Restriction Fragment Length Polymorphisms
(Graner et al. 1991) and PCR-based molecular marker systems like RAPD-
Randomly Amplified Polymorphic DNA (Weyen et al. 1996), SSR-simple sequence
repeats (Pillen et al. 2000; Ramsay et al. 2000; Thiel et al. 2003; Varshney et al.
2006), AFLP-Amplified fragment length polymorphisms (Waugh et al. 1997) and
SNP-single nucleotide polymorphisms (Kota et al. 2001). However, RFLPs are
technically complex, require large quantities of DNA and present a limitation to
high throughput genetic analysis. More recently, trait-linked RFLP markers have
been adapted for PCR amplification, making them amenable to MAS (Tacconi et al.
2006). Marker-assisted breeding is generally more efficient when molecular maps
are saturated, due to an increased chance of finding polymorphic markers in any
genetic background. To date, approximately 1,000 barley SSRs have been published
(Pillen et al. 2000; Struss and Pliescke 1998), of which about one-half have been
genetically mapped (Ramsay et al. 2000; Varshney et al. 2006; Wenzl et al. 2006).

8.5.1 Drought

Barley is characterized by immense variation with respect to drought adaptation and

has been cultivated from boreal to equatorial regions of the world (Schulte et al.
2009). The slow progress in this area is mainly due to quantitative inheritance of
drought-related traits. The advent of molecular tools has made it possible to dissect
genetic inheritance of this trait-complex and several successful QTL analyses have
been performed in barley and related species (El Soda et al. 2010; McKay et al.
8 Molecular Breeding to Improve Plant Resistance to Abiotic Stresses 307

2008; Teulat et al. 2003; Tondelli et al. 2006). These studies revealed that crop
plants have evolved a number of drought-adaptive traits to maintain their life under
water-deficit conditions.

8.5.2 Cold

In the Triticeae genome, the long arm of chromosome 5 has been the region most
frequently reported to be associated with low-temperature tolerance and vernaliza-
tion response (Francia et al. 2004; Vágújfalvi et al. 2003). Until recently, these
genes have been reported as QTL effects because they show complex, rather than
Mendelian inheritance. Most recently, two low temperature tolerance QTLs,
approximately 25 cM apart, were reported in the winter x spring two-rowed barley
population as Nure /Tremois (NxT) (Francia et al. 2004). The Nure/Tremois low-
temperature tolerance Fr-H1 QTL corresponds to the Dicktoo/Morex (DxM) barley
population LT tolerance QTL of Hayes et al. (1997), which in turn is coincident
with VRN and flowering time (heading date) QTLs (Hayes et al. 1997). The NxT LT
tolerance Fr-H2 QTL is syntenous with a LT tolerance QTL in diploid wheat
(Vágújfalvi et al. 2003); COR gene product accumulation QTLs also map to this
position in both species.
Recently, candidate genes have been mapped to these QTL positions. Barley
HvBM5A maps to the VRN-H1 QTL position (Von Zitzewitz et al. 2005), in agree-
ment with the position of TmAP1, the candidate VRN-Am1 gene of diploid wheat
(Yan et al. 2003). It is possible that HvBM5A has pleiotropic effects on VRN
response, flowering time and/or LT tolerance. However, Karsai et al. (2001) have
found that these three traits occur in all possible combinations in barley, suggesting
linkage, rather than pleiotropy, may be responsible for the expression. Beales et al.
(2005) recently mapped the photoreceptor PhyC-a potential candidate for the day
length-influenced flowering time QTL to this region in hexaploid wheat.

8.6 Sorghum and Pearl Millet

Sorghum is the world’s fifth most important cereal crop and is the dietary staple of
more than 500 million people spread in 30 countries. It is grown on 40 million ha in
105 countries of Africa, Asia, Oceania and the Americas. Africa and India account
for the largest share (>70 %) of global sorghum area while USA, India, Mexico,
Nigeria, Sudan and Ethiopia are the major sorghum producers (Ashok Kumar et al.
2011). Pearl millet (Pennisetum glaucum (L.) R. Br., a staple food crop grown under
rainfed conditions on approximately 25 million ha of drought-prone arid and semi-
arid regions in Africa and South Asia (FAO and ICRISAT 1996). Drought stress is
a common feature in both sorghum and pearl millet and can occur any time during
the crop cycle and terminal stress (flowering through grain filling) is more
308 G.J.N. Rao et al.

damaging to the productivity of the crop than stress at the vegetative or preflowering
reproductive stages (Mahalakshmi et al. 1987).

8.6.1 Drought

Sorghum is one of the most drought tolerant grain crops and its rich genetic diver-
sity for stress tolerance makes it an excellent crop model and choice for studying the
genetic and physiologic mechanisms of drought tolerance. However, water stress
affects almost every developmental stage of the sorghum plant and damaging effects
of this stress was more noted when it coincided with various growth stages such as
germination; seedling shoot length, root length and flowering (Khayatnezhad et al.
2010; Rauf 2008).
Drought tolerance in sorghum is a complex trait affected by several interacting
plant and environmental factors. Water loss from plant tissues under drought
conditions results in growth inhibition and in a number of other metabolic and phys-
iological changes including abscisic acid (ABA) accumulation, stomatal closure,
decreased photosynthesis, increase in K+ and Cl− which bind water (Borrell et al.
2001). The growth stage at which moisture stress occurs is very important in deter-
mining the response or reaction of sorghum to water stress. Two distinct drought
responses, namely pre-flowering and post-flowering drought responses, have been
described in sorghum and are probably controlled by different genetic mechanisms
(Rosenow 1987). Although somewhat difficult to combine, some sorghum hybrids
containing both pre- and post-flowering drought tolerance have been developed
(Rosenow et al. 1996).
Drought or any other abiotic stress results in marked reduction of yield and plant
growth; as under inadequate water conditions, photosynthesis will be limited and
consequently, limited availability of photosynthetic assimilates and energy to the
plant, and plants use this limited supply of nutrients to their maximal advantage in
order to survive under stress. Identification and understanding the mechanisms of
drought tolerance in sorghum have been major goals of plant physiologists and
breeders. The desirable traits include prolific root system, ability to maintain stoma-
tal opening at low levels of leaf water potential, high osmotic adjustment and vari-
ous seedling parameters (Rajendran et al. 2011) as under drought-stress conditions,
an urgent need for plants would be to increase the uptake of water, which is usually
more available deep in the soil (Xiong et al. 2006).
Water deficit is sensed by the roots which begin to synthesize ABA within one
hour of the onset of the water stress. ABA is transported via xylem from roots to
leaves within minutes to hours. Root length is an important trait against drought
stress in plant varieties; in general, the variety with longer root growth has greater
resistant to drought (Kaydan and Yagmur 2008; Leishman and Westoby 1994).
Dhanda et al. (2004) reported that the osmotic membrane stability of the leaf seg-
8 Molecular Breeding to Improve Plant Resistance to Abiotic Stresses 309

ment was the most important trait, followed by root-to-shoot ratio and root length
on the basis of their relationships with other traits for drought tolerance. These
water sensitive stages may be exploited to discriminate genotypes on the basis of
their resistance to water stress. Among these critical stages, water stress induced
during the seedling stage has been exploited in various crop species to screen germ-
plasm or breeders populations i.e. wheat (Dhanda et al. 2004), sorghum (Bibi et al.
2010; Gill et al. 2002), maize (Farsiani and Ghobadi 2009; Khayatnezhad et al.
2010) and sunflower (Rauf 2008). The excellent drought characteristics of sorghum
make it one of the most important food and feed crops in the arid and semi-arid
regions of the world.

8.6.2 QTL Mapping

Molecular markers have been used to identify and characterize QTLs associated
with several different traits in sorghum, including plant height and maturity (Pereira
and Lee 1995), characters concerned with plant domestication (Patterson et al.
1995), disease resistance (Gowda et al. 1995; Kebede et al. 2001), drought tolerance
(Tuinstra et al. 1997, 1998) and heat, salinity and flooding (Ali et al. 2011; Ejeta and
Knoll 2007). Several sorghum linkage maps have been established using RFLP and
other DNA markers (Kong et al. 2000; Taramino et al. 1997) and more than 2,400
loci have been mapped on an inter-specific F2 population of Sorghum bicolor × S.
propinquum (Bowers et al. 2000). The average marker density of 0.5 cM or 350 kb
between DNA markers is suitable for fine mapping of genes and QTLs. The high-
density genetic map and its relatively small genome size make sorghum a suitable
species for positional cloning.
In pearl millet, a number of genomic regions are associated with drought toler-
ance in terms of both grain yield and its components. For example, a QTL associ-
ated with grain yield per se and for the drought tolerance of grain yield mapped on
linkage group 2, explained up to 23 % of the phenotypic variation. Some of these
QTLs were common across stress environments whereas others were specific to
only a particular stress environment. All the QTLs that contributed to increased
drought tolerance did so either through better than average maintenance (compared
to non-stress environments) of harvest index, or harvest index and biomass produc-
tivity. In addition, a number of genomic regions associated with traits that determine
GY under stress have also been identified, but they were often not associated with
either better maintenance of GY or with actual GY under stress. It was concluded
that there is considerable potential for marker-assisted backcross transfer of selected
QTLs to the elite parent of the mapping population and for their general use in the
improvement of pearl millet productivity in water-limited environments (Yadav
et al. 2002).
310 G.J.N. Rao et al.

8.7 Conclusions and Prospects

Considering the importance of cereal crops as a predominant source of food around

the world, identification of traits and genotypes associated with tolerance to stresses
is vital for the crop improvement programs. The response to abiotic stresses such as
drought, salinity, heat, cold and submergence are regulated by QTLs/
genes/transcription factors etc., to provide stress tolerance in plants. Concerted
efforts are required to fully understand the physiological and molecular basis of
tolerance and emphasis should be on discovering potential candidate genes through
evaluation of the genetic resources available followed by characterization, mapping
and cloning. Functional analysis of these genes and transcription factors will thus
provide more information on the intricate regulatory network pathways involved in
abiotic stress responses and the cross-talk between different signaling pathways
during stress adaptation. This will provide a clearer understanding of abiotic stress-
related signal transduction events. The development of molecular genetic markers
and the use of these markers in QTL analysis is increasingly becoming a common
approach for accelerating gains from selection for complex quantitative traits in
crop plants in breeding programs. However, lack of stability across different envi-
ronments and QTL × E interaction evaluation remains a major impediment to the
efficient use of MAS and further progress in the area can lead to a better understand-
ing of the mechanisms involved and with the availability of precise markers, the
transfer of the traits into desirable backgrounds will be quicker, easier and simpler.
The identified QTLs, genes and transcription factors can also be genetically engi-
neered to produce transgenic plants to confer higher levels of tolerance to various
abiotic stresses. Further improvements in the area of QTLs and candidate genes/
alleles will lead to development of crop varieties having superior levels of stress
tolerance as crop improvement programs will have high precision.


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