Improving Salt Tolerance in Rice: Looking Beyond the Conventional

  • K. K. Vinod
  • S. Gopala Krishnan
  • N. Naresh Babu
  • M. Nagarajan
  • A. K. Singh
Chapter

Abstract

Several factors in the intensive cropping system have played significant role in deteriorating soil health in general. soil salinization is one of the major issues threatening crop productivity in major irrigated rice growing areas of the world. Salinity is a serious issue in rice, the crop that feeds half the world, since it is sensitive to salt accumulation. With the world population growing incessantly, there is an urgent need to increase rice productivity especially in salinized lands as well as to reutilize lands that are rendered unproductive due to salt accumulation. It is therefore essential to develop varieties that are phenologically capable of sustaining excess salt throughout its life span and produce higher yield. Although there is sufficient variability in rice germplasm for salt tolerance, conventional breeding has been far less fruitful in addressing this complex problem. With the deeper understanding of the intricate mechanisms of salt tolerance and the array of genes and useable quantitative trait loci that are being discovered, the breeding scenario towards salt tolerant rice is poised to take a more productive turn in near future. This chapter outlines the latest developments in rice breeding towards salt tolerance through employment of modern molecular techniques in conjunction with the conventional breeding approaches.

Keywords

Soil salinity Rice Molecular genetics Salt tolerance Molecular breeding 

Salinity is one of the major factors limiting productivity of crops including rice around the world. Soil salinity is often accompanied by osmotic imbalance, mineral deficiency and toxicity that has adverse effects on crop growth (Parvaiz and Satyawati 2008, Ahmad 2010; Ahmad et al. 2010, 2011, 2012a; Ahmad and Prasad 2012a, b). Although the term salinity in general refers to adverse effects of salt accumulation in soils, in strict sense there are two broad types of salt problem soils (a) alkaline (sodic) and (b) saline. Alkaline or sodic soils have appreciable quantities of sodium and ions capable of alkaline hydrolysis such as carbonates with exchangeable sodium percent (ESP) of more than 15% coupled with a pH above 8.2 and an average root-zone electrical conductivity of saturated soil extract (ECe) of less than 4 dS m−1 (approx. 40 mM NaCl) and poor soil structure. Whereas, saline soils are predominant with neutral salts of sulphates and chlorides of sodium, calcium and magnesium with ECe of 4 dS m−1 or more, pH less than 8.2 and ESP lower than 15% (Richards 1954). Soil salinization is gradual and occurs naturally, anthropogenically or by a combination of both (secondary salinization). Most common factors that influence soil salinization are, excessive irrigation without proper drainage in inlands (Borlaug and Dowswell 2005), underlying rocks rich in harmful salts, use of saline ground water, saline seeps triggered by deforestation and shift in cropping pattern, sea water ingression, water balance disturbance due to irrigation, localized redistribution of salts, excessive evaporation over precipitation, anaerobic reduction under high organic matter and climate change. Recent mega-tsunamis that affected many South and Southeast Asian countries and Japan had engrossed several million acres of land rendering them salt affected (Chandrasekharan et al. 2008; Abe et al. 2012).

Soil Salinity in Rice Growing Regions of the World

More than 6.2% of the total world area amounting to 837 million hectares (M ha) is salt affected (Fisher et al. 2002), of which roughly about 48% is saline and 52% is sodic (Bot et al. 2000) with saline soils predominating major rice areas of the world (Fig. 10.1). Area under salt stress is on the rise with an estimated 10–40 M ha becoming salinized every year due to secondary salinization that renders vast areas of land un(der) utilized (Pessarakli and Szabolcs 1999; Ahmed and Qamar 2004; Ansari et al. 2007). Published estimates show that more than 76 M ha of land worldwide has become salt-affected due to secondary salinization of which about 45 M ha is irrigated (Dregne et al. 1991; Oldeman et al. 1991).
Fig. 10.1

Worldwide distribution of sodic and saline soils showing prominence of saline soils in major rice growing regions of South and Southeast Asia

Rice is cultivated in more than 115 countries, of which Asia’s share is more than 91% of the world total. Majority of the Asian rice production zone is confined to South and South East Asia wherein severe salinity related problems are rampant in 20% of the area amounting to 47 M ha (Abbas et al. 1994) consisting of warm humid coastal regions and marshy inlands (Fig. 10.2). India and Pakistan has the largest share of area under salinity among the South Asian nations (Table 10.1). About 7% of India’s land area amounting to 21 M ha and 20% of the land area (16 M ha) in Pakistan are salt affected. In India, salinity coupled with waterlogging is seriously threatening agricultural economy in Indo-Gangetic plains covering the states of Haryana, Punjab and Uttar Pradesh. In Pakistan, reports indicate that more than 1 M ha rice area is salt affected with 25–60% reduction in production (Haq et al. 2010) and more than 1.4 M ha land is abandoned due to salinity (World Bank 2006).
Table 10.1

Distribution of saline and sodic soils in major rice growing countries of South and Southeast Asia

Country

Area in million hectares (M ha)

Salinity

%

Sodicity

%

Total

Bangladesh

0.9

6.3

0.0

0.0

14.4

Cambodia

0.2

1.1

0.4

2.2

18.1

India

21.0

6.7

1.5

0.5

315.7

Indonesia

2.1

1.1

0.0

0.0

191.6

Laos

0.0

0.0

0.1

0.4

23.7

Malaysia

1.0

3.0

0.0

0.0

33.3

Myanmar

1.1

1.6

0.0

0.0

67.7

Pakistan

15.8

19.7

0.1

0.1

80.2

Papua New Guinea

0.4

0.9

0.0

0.0

46.2

Philippines

0.0

0.0

0.0

0.0

29.9

Sri Lanka

0.1

1.5

0.5

7.7

6.5

Thailand

1.0

1.9

0.4

0.8

51.3

Viet Nam

0.7

2.1

0.0

0.0

32.9

World

402.5

3.0

434.4

3.2

13,490.7

Data from Bot et al. (2000)

Fig. 10.2

Distribution of saline soils in Asia (in colored patches), with demarcation (dotted) showing 91% of the rice growing areas of the world confined to South and Southeast Asia

Salinity is a common problem along the coastal belts of rice growing countries, especially in India. Such areas are characterized by occasional or frequent sea water ingression during tides resulting in submergence that builds up salt accumulation. Rice is the only viable crop in these areas because it can withstand submergence and shows wide variability for salt tolerance. However, under salt prone conditions, yield is reduced from 10% to 80%, and coupled with erratic rainfall, loss can reach up to 100%. Further, low productivity can also be attributed to occasional flooding, rainfed rice cultivation, frequent water-deficit stress and continued cultivation of traditional low-yielding rice varieties and landraces (Singh et al. 2009). In near future, Asia requires more rice to feed its burgeoning population, since rice is the staple food for more than 90% of Asians. Ironically, millions of hectares of rice cultivable areas are either being rendered uncultivable or are grown with very low yields because of growing soil salinization. Two options to recover more out of such problem areas are reclaiming soil off the salinity and by cultivating salt tolerant varieties. The second option seems more feasible and sustainable, as there is enough variability in the rice germplasm for salt tolerance which could be utilized in rice breeding against soil salinity.

Salt Stress in Rice

Rice is sensitive to salinity, particularly during the seedling stage (Maas and Hoffman 1977) and the earlier set benchmarks (Maas and Grattan 1999; Hanson et al. 1999) indicate that rice yield decreases 12% for every unit (dS/m) increase in ECe above the threshold tolerance of 3.0 dS m−1(Maas 1990). Salt sensitivity in rice is now revised to a much lower threshold tolerance of 1.8 dS m−1 with yield decline slope of 9.1% (Grattan et al. 2002). Salinity affects yield components such as panicle length, spikelet number per panicle, and grain yield (Zeng and Shannon 2000), besides delayed panicle emergence and flowering, and reduced seed set percentage due to lower pollen viability (Khatun and Flowers 1995).

As against the earlier belief that the salt induced damage in rice is caused by osmotic imbalance and accumulation of chloride (Cl) ions (Tagawa and Ishizaka 1963), it is now known that injury is primarily caused by sodium ion (Na+) toxicity due to cellular ion imbalance (Mandhania et al. 2006). In contrast to adverse effect on root growth, presence of excess amounts of Na+ results in greater reduction in shoot growth and yield (Esechie et al. 2002). When compared to other cereals, Cl ions are relatively well tolerated by rice at varying concentrations preempting them being toxic (Clarkson and Hanson 1980). Rice plants uptake excess levels of Na+ under salt rich conditions, interfering with the uptake of potassium (K+) and calcium (Ca2+) inciting deficiency symptoms. Low K+ uptake result in high Na+/K+ ratio within plants, which together with low Ca2+ uptake causes impairment of mineral transport resulting in reduced shoot growth. The rate of conversion of soluble sugars into starch is reduced concomitantly with the reduced uptake of K+, as K+ is needed for the catalytic activities of starch biosynthesis enzymes (Zhang et al. 2012). Further, decrease in carbohydrate accumulation under severe salt stress may also occur due to reduced carbon assimilation (Moradi and Ismail 2007; Pattanagul and Thitisaksakul 2008) resulting from the damage of photosynthetic machinery (Moradi and Ismail 2007). Photoinhibition along with salt stress can cause serious damage to photosynthesis, nutrient uptake, water absorption, root growth and cellular metabolism leading to yield loss (Hasegawa et al. 2000; Zeng and Shannon 2000; Zhu 2001). Besides, salt stress rapidly activates several lipid responses in rice leaves, however, whether these responses do have any role in salt tolerance is not clear (Darwish et al. 2009). Further, on long term exposure to salinity, especially during development, morphological modifications may be seen occurring in leaves by development of smaller and densely packed cells with thickened cell walls (Qiu et al. 2007).

Rice cultivars show variable sensitivity towards salinity at different phenological stages, with better tolerance during germination and tillering (Khan et al. 1997). Tolerance drops significantly at young seedling stage and especially during early reproductive stage becoming very sensitive during panicle initiation and fertilization, directly affecting the crop yield (Heenan et al. 1988; Zeng et al. 2001). A possible reason for this variability is the ability of rice plants to grow in standing water that can dilute and leach away excess salts in the soil (Bhumbla and Abrol 1978). Particularly due to the early seedling susceptibility, older seedlings are generally recommended for transplanting into saline soils. Young rice plants of susceptible varieties die after germination, while those of the adapted survive showing reduced growth, together with osmotic adjustments to avoid dehydration. Seedling biomass is now recognized as an important parameter for the survival of transplanted seedlings in saline soils (Summart et al. 2010). However, there are reports in which rice varieties show poor correlation of seedling and adult plant salt tolerance (Moradi et al. 2003), which can pose a major challenge because combinatorial expression of tolerance sustaining throughout the crop lifespan is essential for breeding tolerant varieties (Ismail et al. 2007). Therefore, most of these reports are only suggestive because the earlier investigations on salt tolerance are done on seedlings grown under hydroponics, tissue culture environment, and under artificial salinization of the culture media. Although artificial screening may simulate near perfect situations of salt sufficiency, it may fail to duplicate natural situations that are practically relevant for breeding.

Physiological Basis of Salt Tolerance in Rice

Salt tolerance in rice, is an integrated phenomenon contributed by several traits relating to water and mineral uptake, transpiration, osmotic balance, tissue tolerance, oxidant scavenging and growth vigor (Moradi et al. 2003). Physiological basis of salt tolerance in rice plants is primarily manifested by Na+ exclusion from young tissues and flag leaves and developing panicles (Asch et al. 2000; Haq et al. 2010). High Na+ concentration in the apoplastic solution results in increased accumulation of proline in the cytoplasm especially in tolerant rice genotypes, which helps in restoring the osmotic potential between the cytosol and apoplastic solution (Demiral and Turkan 2005). A comprehensive review of mechanisms of salt tolerance (Munns and Tester 2008) with major focus on rice (Ismail et al. 2007; Negrão et al. 2011) can be found elsewhere. Other mechanisms operating in rice include confining of toxic ions to older leaves and vacuoles, secondary responses such as scavenging reactive oxygen species (ROS), enhanced growth response to dilute salts and increased stomatal response. Salt stress was reported to increase chlorophyll concentration in leaves of tolerant and moderately tolerant rice genotypes, with significant levels of chlorophyll a concentration and high chlorophyll a/b ratio. Being the major photosynthetic pigment, reduction in chlorophyll a may be associated with reduced photosynthetic activity under salt stress (Moradi and Ismail 2007). Salt induced inhibition of conversion of soluble sugars into starch was less in salt tolerant genotypes (Zhang et al. 2012). Additionally, long-term reduction of mesophyll conductance under salt stress results in anatomical modifications in leaves (Chaves et al. 2009).

In a recent investigation to identify biochemical markers for salt tolerance, significantly reduced level of H2O2 activity was observed in the tolerant variety Pokkali, suggesting the existence of an efficient antioxidant defense system to cope up with salt-induced oxidative stress. Supporting this hypothesis, higher activities of antioxidant enzymes and isozyme patterns that are either directly or indirectly involved in the detoxification of ROS, were observed in Pokkali. Further, Pokkali exhibited a higher reduced versus oxidized glutathione ratio (GSH/GSSG) together with a higher ratio of reduced versus oxidized ascorbate ratio and higher activity of methylglyoxal detoxification system (glyoxalase I and II). As reduced glutathione is involved in the ascorbate–glutathione pathway as well as in the methylglyoxal detoxification pathway, the results suggest that both ascorbate and glutathione homeostasis, which is also modulated via glyoxalase enzymes, can be considered as biomarkers for salt tolerance in rice (El-Shabrawi et al. 2010). In salt tolerant genotypes of rice, activity of enzymes such as ascorbate peroxidase, catalase and peroxide dismutase, that are known to be involved in ROS scavenging was found to be either constitutively expressed or induced by salt stress (Moradi and Ismail 2007; Nagamiya et al. 2007; Ahmad et al. 2008).

Genetics of Salt Tolerance in Rice

Genetic Variability and Inheritance of Salt Tolerance

Rice genetic diversity harbors natural variability for salt tolerance. In a large scale screening of rice genotypes conducted at the International Rice Research Institute (IRRI), about 17% of the total 1,38,000 genotypes have been found to possess acceptable levels of salt tolerance (EC 10 dsm−1) at seedling stage (De Datta et al. 1993). A basic understanding on the genetics and relationships between varietal groups and phenotypic variation for salt tolerance is vital for bioprospecting of genes and mining useful alleles. Till date, there have been no systematic studies for comparing within and between group variability for salt tolerance in rice. Several independent studies have reported many landraces and varieties tolerant to salt accumulation by one mechanism or another (Gregorio et al. 2002; Ismail et al. 2007; Mohammadi-Nejad et al. 2010). However, most of the traditional salt tolerant varieties from coastal regions of India such as pokkali rice types (Pokkali, Cheruvirippu, Bali, Orkayama, Eravapandy, Orpandy, Oorumundakan, Chettivirippu, Kuruka, Anakodan, Chottupokkali etc.) from Kerala and Nona Bokra, Getu, Kalarata 1–24, SR26B, Damodar, Dasal, Patnai and Nona Sail from West Bengal possess undesirable agronomic and grain quality characters. Other salt tolerant indica cultivars grown traditionally in the coastal areas of other countries include Kalimekri, Bhirpala, Kajalsail (Bangladesh), Ketumbar, Kuatik Putih (Indonesia), Khao Seetha (Thailand) and Soc Nau (Vietnam). Several breeding lines have been developed at the IRRI with specific characteristic features for salt tolerance namely IR4630-22-2-5-1-3 (a donor for leaf compartmentation), IR60167-129-3-4 (a donor for tissue tolerance), and IR66946-3R-178-1-1 (also known as FL478). Similarly, popular salt tolerant varieties such as CSR10, CSR13, CSR27 and CSR30 have been developed and released from the Central Soil Salinity Research Institute (CSSRI) at Karnal in India using traditional salt tolerant varieties as parent (Negrão et al. 2011).

Hardly little was known about inheritance of salt tolerance in rice until 1970s, when Akbar and Yabuno (1977) reported that panicle sterility under salt stress was a dominant trait controlled by a small number of genes. Later, overdominance of salt tolerance was demonstrated in crosses between tolerant and susceptible varieties, accompanied by dominance and a sizeable degree of fixable additive variance (Moeljopawiro and Ikehashi 1981). Subsequent genetic studies indicated that salt tolerance in rice was a complex trait under polygenic control (Flowers 2004) with large environmental effects and low heritability (Gregorio and Senadhira 1993). However, in crosses with moderately tolerant and susceptible parents, duplicate type of epistasis was also reported (Ray and Islam 2008). It is rather difficult to consolidate and quantify genetic effects of tolerant traits since screening methods for tolerance were different at different growth stages and hardly any relation exists between phenological tolerance expressions. Nevertheless, considerable variation for difference in survival traits and components of salt injury are reported coupled with significant genotype  ×  environment interactions (Zhou et al. 2010; Ali et al. 2006). Many workers have attempted genetic component analysis on various traits, especially on Na+/K+ compensation, and reported both additive and dominant gene effects and overdominance (Gregorio and Senadhira 1993; Ray and Islam 2008). Agronomic performance under salinity showed preponderance of dominant gene action for yield components and additive gene action for morphological traits (Kalaiyarasi et al. 2002; Sankar et al. 2008). Recent mixed model genetic analysis (Wang et al. 2010) on seed germination under salinity, reported polygenic control of the component traits with preponderance of two to three major genes showing high heritability and accounting for 12.5–99.0% of the total phenotypic variation. A specific genetic model was fitted for each trait, that showed control of two major genes on imbibition rate, two major genes plus polygene on germination and vigor indices, three major genes plus polygene on germination rate and two major genes or two major genes plus polygene on shoot and root length. Significant dominant effects and absence of epistasis for salt tolerant traits have also been reported suggesting the possibility of hybrid rice development under saline situations (Ray and Islam 2008) and using modified bulk and single seed descent methods with later generation selections using larger population as breeding strategies (Gregorio and Senadhira 1993).

Molecular Genetics

Molecular mechanisms triggered in plants’ defense against salt stress may be based on either avoidance or tolerance strategies. Selective ion uptake, dilution of excess ions, sequestration and extrusion are the major avoidance mechanisms, manifested at cellular, organellar or whole-plant levels. Moreover, plants have an array of tolerance mechanisms to sustain growth under unfavorable conditions, triggering a cascade of systemic reactions related to salt injury that jeopardize osmotic balances, photorespiration, mineral transport, membrane stability, cell division, cell architecture organization and survival. Therefore most of the defensive genes against salt injury may share common profile of other abiotic stresses (reviewed by Bartels and Sunkar 2005; Chaves et al. 2003; Munns and Tester 2008; Witcombe et al. 2008; Singh et al. 2008; Peleg et al. 2011; Negrão et al. 2011; Krasensky and Jonak 2012). In rice, several genes have been functionally validated for salt tolerance, many of which are sourced from other systems (Table 10.2), besides rice genes (Table 10.3).
Table 10.2

External genes functionally tested in transgenic rice for imparting salt tolerance

Code

Encoded protein

Source organism

Promotor

Associated trait

References

HVA1

LEA protein

Hordeum vulgare

Rice Actin1

Stress response

Xu et al. (1996)

P5CS

Δ1-pyrroline-5-carboxylate synthetase

Vigna aconitifolia

Stress-inducible

Proline accumulation

Zhu et al. (1998)

codA

Choline oxidase

Arthrobacter globiformis

CaMV 35S

Glycinebetaine synthesis

Sakamoto et al. (1998)

MnSOD

Superoxide dismutase

Saccharomyces cerevisiae

Antioxidants synthesis

Tanaka et al. (1999)

mtlD, gutD

Mannitol-1-phosphate dehydrogenase

Escherichia coli

CaMV 35S

Sugar alcohol synthesis

Wang et al. (2000)

Glucitol-6-phosphate dehydrogenase

ADC

Arginine decarboxylase

Avena sativa

ABA inducible

Polyamine activity

Roy and Wu (2001)

SAMDC

S-adenosylmethionine decarboxylase

Tritordeum

ABA inducible

Polyamine synthesis

Roy and Wu (2002)

codA

Choline oxidase

Arthrobacter globiformis

CaMV 35S

Glycinebetaine synthesis

Mohanty et al. (2002)

AgNHX1

Na+/H+ antiporter1

Atriplex gmelini

CaMV 35S

Na+ homeostasis

Ohta et al. (2002)

otsA, otsB

Trehalose biosynthetic genes

Escherichia coli

CaMV 35S, rice rbcS

Trehalose accumulation

Garg et al. (2002)

HVA1

LEA protein

Hordeum vulgare

Rice Actin1

Stress response

Rohila et al. (2002)

TPS, TPP

Trehalose biosynthetic genes

Escherichia coli

Ubiquitin1

Trehalose accumulation

Jang et al. (2003)

δ-OAT

Ornithine-δ-aminotransferase

Arabidopsis thaliana

CaMV 35S

Proline accumulation

Wu et al. (2003)

P5CS

Δ1-pyrroline-5-carboxylate synthetase

Vigna aconitifolia

CaMV 35S

Proline accumulation

Su and Wu (2004)

CN Atr

Calcineurin

Mouse

CaMV 35S

Ion homeostasis

Ma et al. (2005)

AtMYB2

MYB transcription factor

Arabidopsis thaliana

AIPC

Stress response

Malik and Wu (2005)

CBF3, ABF3

ABA independent CBF3/DREB1A

Arabidopsis thaliana

Ubiquitin1

Stress response

Oh et al. (2005)

nhaA

Na+/H+ antiporter

Escherichia coli

CaMV 5S

Ion homeostasis

Wu et al. (2005)

DREB1A, DREB1B, DREB1C

Dehydration responsive element binding (DREB)

Arabidopsis thaliana

CaMV 5S, Ubiquitin

Dehydration response

Ito et al. (2006)

GST, CAT

Glutathione S-transferase, Catalase

Suaeda salsa

CaMV 35S

Antioxidant activity

Zhao and Zhang (2006)

SOD2

Sodium2

Schizosaccharomyces pombe

CaMV35S

Na+ homeostasis

Zhao et al. (2006a)

SsNHX1, AVP1

Vacuolar membrane Na+/H+ antiporter, Vacuolar H+ pyrophosphatase proton pump

Suaeda salsa, Arabidopsis thaliana

CaMV35S

Na+ homeostasis

Zhao et al. (2006b)

codA

Choline oxidase

Arthrobacter pascens

ABA inducible

Glycinebetaine synthesis

Su et al. (2006)

katE

Catalase

Escherichia coli

CaMV 35S

Antioxidant activity

Nagamiya et al. (2007)

HvCBF4

CBF transcription factor

Hordeum vulgare

Ubiquitin1

Cold tolerance

Oh et al. (2007)

PgNHX1

Vacuolar Na+/H+ antiporter

Pennisetum glaucum

ABA inducible

Na+ homeostasis

Verma et al. (2007)

Cu/Zn SOD1

Superoxide dismutase

Avicennia marina

Ubiquitin

Antioxidative pathway

Prashanth et al. (2008)

TERF1

Tomato ethylene responsive factor

Lycopercicum esculentum

CaMV 35S

Stress regulatory

Gao et al. (2008)

NtOPBP1

Osmotin promoter binding protein 1

Nocotiana tabacum

Ubiquitin

Salt tolerance

Chen and Guo (2008)

TaSTRG

Salt tolerance-related gene

Triticum aestivum

Actin

Salt stress response

Zhou et al. (2009)

AtHKT1;1

High affinity K+ transporter

Arabidopsis thaliana

Root specific

Na+ homeostasis

Plett et al. (2010)

P5CSF129A

Δ1-pyrroline-5-carboxylate synthetase

Vigna aconitifolia

CaMV 35S

Proline accumulation

Kumar et al. (2010)

PgNHX1

Vacuolar Na+/H+ antiporter

Pennisetum glaucum

CaMV 35S

Na+ homeostasis

Islam et al. (2010)

P5CS

Δ1-pyrroline-5-carboxylate synthetase

Vigna aconitifolia

CaMV 35S

Proline accumulation

Karthikeyan et al. (2011)

PDH45

DEAD-box helicase

Pisum sativum

CaMV 35S

Salt stress response

Amin et al. (2012)

Table 10.3

Rice genes that are functionally tested for improved salt tolerance through transgenesis

Gene

Encoded protein

Transgene candidate

Promotor

Associated trait

References

OsCDPK7

Calcium-dependent protein kinase

Oryza sativa

CaMV 35S

Cytosolic Ca2+ influx

Saijo et al. (2000)

GS2

Chloroplastic glutamine synthetase

Oryza sativa

CaMV35s

Photorespiration

Hoshida et al. (2000)

OsMAPK5a

Mitogen-activated protein kinase

Oryza sativa

Ubiquitin

Cytosolic Ca2+ influx

Xiong and Yang (2003)

OsDREB1A

DREB Transcription factor

Arabidopsis thaliana

CaMV35s

Dehydration response

Dubouzet et al. (2003)

OsNHX1

Na+/H+ antiporter

Oryza sativa

CaMV 35S

Na+ homeostasis

Fukuda et al. (2004)

OsMAPK44

Mitogen-activated protein kinase

Oryza sativa

Cytosolic Ca2+ influx

Jeong et al. (2006)

OsDREB1A, OsDREB1B

Dehydration responsive element binding (DREB)

Oryza sativa

Ubiquitin

Dehydration response

Ito et al. (2006)

SNAC1

Stress-responsive NAC 1

Oryza sativa

CaMV 35S

Stress response

Hu et al. (2006)

OsSOS1

Salt overlay sensitive

Arabidopsis thaliana

CaMV 35S

Na+ homeostasis

Martinez-Atienza et al. (2007)

Rab16A

Responsive to ABA dehydrins

Nicotiana tabacum

Rab16A

Dehydration response

RoyChoudhury et al. (2007)

OsNHX1

Vacuolar type Na+/H+ antiporter

Oryza sativa

CaMV 35S

Na+ homeostasis

Chen et al. (2007)

OsCIPK12

Calcineurin B-like protein-interacting protein kinase

Oryza sativa

Ubiquitin

Cytosolic Ca2+ influx

Xiang et al. (2007)

OsKAT1

Shaker family K+ channel

Oryza sativa

CaMV 35S

K+ uptake

Obata et al. (2007)

OsAPXa, OsAPXb

Ascorbate peroxidase

Oryza sativa

CaMV 35S

Antioxidant activity

Lu et al. (2007)

OsNAC6

NAC transcription factor

Oryza sativa

Ubiquitin

Stress response

Nakashima et al. (2007)

glyII

Glyoxalase II

Oryza sativa

CaMV 35S

Salt tolerance

Singla-Pareek et al. (2008)

OsTOP6A1

Meiotic recombination protein

Arabidopsis thaliana

CaMV 35S

Multiple stress response

Jain et al. (2008)

OsiSAP8

Stress associated protein

Nicotiana benthamiana

CaMV 35S

Multiple stress response

Kanneganti and Gupta (2008)

OsiSAP8

Stress associated protein

Oryza sativa

CaMV 35S

Multiple stress response

Kanneganti and Gupta (2008)

OsHsfA2e

Heat shock transcription factor

Arabidopsis thaliana

CaMV 35S

Stress response

Yokotani et al. (2008)

ZFP252

TFIIIA-type zinc finger protein

Oryza sativa

CaMV 35S

Proline accumulation

Xu et al. (2008)

OsTPP1

Trehalose-6-phosphate phosphatase

Oryza sativa

CaMV 35S

Trehalose accumulation

Ge et al. (2008)

SNAC2

Stress-responsive NAC

Oryza sativa

Ubiquitin, Ubi1

Stress response

Hu et al. (2008)

ONAC063

NAC transcription factor

Arabidopsis thaliana

CaMV 35S

 

Yokotani et al. (2009)

ONAC045

Stress-responsive NAC

Oryza sativa

CaMV 35S

LEA gene expression

Zheng et al. (2009)

AP37

APETALA 2 transcription factor

Oryza sativa

OsCC1

Stress regulatory

Oh et al. (2009)

DST

Ethylene zinc finger protein

Oryza sativa

CaMV 35S

Stomatal control

Huang et al. (2009)

OsSIK1

Receptor-like kinase

Oryza sativa

OsSIK1

Antioxidant activity

Ouyang et al. (2010)

OsNAC10

Stress-responsive NAC

Oryza sativa

GOS2, RCc3

Stress response

Jeong et al. (2010)

OsNAC5

Stress-responsive NAC

Oryza sativa

Ubiquitin

LEA gene expression

Takasaki et al. (2010)

ZFP179

Cys2/His2-type zinc finger protein

Oryza sativa

CaMV 35S

Proline accumulation

Sun et al. (2010)

OsNHX1

Na+/H+ exchanger

Oryza sativa

CaMV 35S

Osmoregulation system

Liu et al. (2010b)

OsVP1

H+-pyrophosphatase in tonoplasts

Oryza sativa

CaMV 35S

Na+ homeostasis

Liu et al. (2010b)

OsTPKb

Two pore K+ channel

Oryza sativa

CaMV 35S

K+ homeostasis

Mian (2010)

OsAKT1

K+ inward rectifying channel

Oryza sativa

CaMV 35S

K+ uptake

Mian (2010)

OsTPS1

Trehalose-6-phosphate synthase

Oryza sativa

Actin1

Trehalose accumulation

Li et al. (2011)

OsHAK5

Sodium-insensitive potassium transporter

Nicotiana tabacum

CaMV 35S

K+ transport

Horie et al. (2011b)

OsNAC5

Stress-responsive NAC

Oryza sativa

CaMV 35S

Proline accumualtion

Song et al. (2011)

OsHsfC1b

Heat shock factors

Oryza sativa

Ubiquitin

Stress response

Schmidt et al. (2012)

Monovalent ion transport such as that of K+, Na+ and Cl are governed by ion channel and carrier proteins and their isoforms that are encoded by large multi-gene families. When encountered with salt stress, these transporters play crucial roles in uptake, efflux, translocation and sequestration. Main classes of ion channel proteins are non-selective cation channels (NSCC), two-pore K+ channels (TPK), shaker proteins and voltage gated Cl channels (CLC). They include sub-forms such as cyclic nucleotide gated channel (CNGC), glutamate like receptor (GLR), and shaker type K+ inward rectifying channels (KIRC) and outward rectifying channels (KORC). The carrier proteins include (a) symporters and their sub-forms such as cation chloride co-transporter (CCC), K+ uptake permease (KUP) and high affinity K+ transporters (HKT), and (b) antiporters that include Na+/H+ exchangers (NHX), cation/H+ exchangers (CHX), K+/H+ exchangers (KHX) and salt overlay sensitive (SOS) gene families (Szczerba et al. 2009). Primary mechanism of salt tolerance in plants is now known to be manifested by ion exclusion mechanisms, especially of Na+, in association with osmo-regulation, in which physiological friendly solutes such as sugars (trehalose, fructan), sugar alcohols (galactinol, trehalose and mannitol), amino acids (proline) and amines (glycine betaine) are accumulated in the plant systems to ward off the ill effects of accumulating solutes. Besides, several transcription factors (TF) and their cis-regulatory sequences act as molecular switches of stress response gene expression at temporal and spatial levels (Puranik et al. 2012).

The HKT Gene Family

Na+-K+ homeostasis governs the principal mechanisms of salt tolerance in plants such as ion uptake and transport, sequestration and extrusion. The major genes involved in Na+ uptake under saline conditions are governed by HKTs, while vacuolar Na+/H+ antiporters regulate Na+ sequestration in vacuoles and membrane Na+/H+ antiporters regulate Na+ extrusion as seen in halophytes (Yamamoto and Yano 2008). Plant HKTs represent a class of xylem–parenchyma-expressed Na+-permeable genes that govern primary mechanism mediating salt tolerance and Na+ exclusion from leaves. HKT genes are the most widely studied genetic system for salt tolerance in Arabidopsis, and in rice they constitute a large gene family of nine genes consisting of two distinctly grouped sub-families of OsHKT1 with five genes (Garciadeblás et al. 2003; Platten et al. 2006; Huang et al. 2008b) and OsHKT2 containing four genes (Table 10.4). Although named after their relation with bacterial high affinity K+ transport genes, HKT genes are primarily Na+ transporters and regulates a variety of cellular mechanisms such as Na+ sequestration, extrusion and exclusion (Hauser and Horie 2010) and play a key role in regulation of Na+ homeostasis (Rodríguez-Navarro and Rubio 2006). Evidences show that OsHKT1 genes distinctly act as Na+ uniporters and OsHKT2 as Na+-K+ symporters or uniporters depending on the ionic conditions (Huang et al. 2008b; Pardo 2010). A detailed review of HKT transporter-mediated salt tolerance mechanisms can be found at Horie et al. (2009) and Hauser and Horie (2010).
Table 10.4

High affinity potassium transporters (HKT) on rice reference genome cv. Nipponbare

Gene

Chromosome

Genome location

Other names

Length (bp)

No. of transcripts

OsHKT1;1

4

LOC_Os04g51820

OsHKT4

2,443, 2,224, 2,097

3

OsHKT1;2

4

OsHKT5

Pseudogene

OsHKT1;3

2

LOC_Os02g07830

OsHKT6

1,733

1

OsHKT1;4

4

LOC_Os04g51830

OsHKT7

2,269

1

OsHKT1;5

1

LOC_Os01g20160

OsHKT8, SKC1

2,164

1

OsHKT2;1

6

LOC_Os06g48810

OsHKT1

1,881

1

OsHKT2;2

?

OsHKT2

OsHKT2;3

1

LOC_Os01g34850

OsHKT3

1,628

1

OsHKT2;4

6

LOC_Os06g48800

OsHKT9

1,557

1

HKT transporters fulfill distinctive roles at the whole plant level in rice, each system playing decisive roles in different cell types. OsHKT1;5 (OsHKT8), was the first among the HKT genes to be mapped, identified initially as a quantitative trait locus (QTL), shoot K+content 1 (SKC1; Lin et al. 2004). Functional analysis later identified SKC1 to code for a transporter that unloads Na+ from the root xylem and preferentially expressed in the parenchyma cells surrounding xylem vessels. It was postulated that relative salt tolerance of rice landraces Pokkali and Nona Bokra is due to the presence of OsHKT1;5 (Ren et al. 2005). OsHKT1;1 and OsHKT1;3 are exclusively permeable to Na+ and are expressed in roots and leaves, suggesting more wider functional role other than ion transport. These transporters may be involved in ion fluxes triggering turgor changes in bulliform cells that control leaf rolling and unrolling, allowing them to regulate leaf folding in response to environmental conditions (Jabnoune et al. 2009). Although OsHKT1;4 sequences has a structural synteny with Na+exclusion 1 (Nax1) gene conferring salt tolerance in durum wheat (Huang et al. 2006), that is preferentially expressed in shoot (Garciadeblás et al. 2003), no QTL for salt tolerance was detected on its locus on rice chromosome 4, suggesting that it may either be silenced or unexpressed in rice (James et al. 2011). OsHKT1;2 is identified as a pseudogene in Nipponbare genome and no functional properties are reported for this gene so far.

Depending on the ionic conditions, members of HKT2 transporter subfamily were found to mediate Na+-K+ symport under normal concentrations and Na+-selective transport under high Na+ concentrations. OsHKT2;1 was a highly conserved protein (Oomen et al. 2012) that is expressed strongly in roots, and weakly in mesophyll cells of mature leaves, displaying three conducting modes depending on external Na+ and K+, K+-Na+ symport, Na+ and K+ uniport (Jabnoune et al. 2009). The second member of the family, OsHKT2;2 is demonstrated to act as Na+-K+ symporter in tobacco cells (Yao et al. 2010). Recently an isoform of OsHKT2;2 (No-OsHKT2;2/1) that is likely to have originated from a deletion in chromosome 6, producing a chimeric gene is identified in Nona Bokra, a highly salt-tolerant cultivar (Oomen et al. 2012). It has a 5′ region corresponds to that of OsHKT2;2, as found in Pokkali but with a 3′ region corresponds to that of OsHKT2;1. In contrast to OsHKT2;1, No-OsHKT2;2/1 is essentially expressed in roots and displays a significant level of permeability to Na+ and K+ even at high external Na+ concentrations. No-OsHKT2;2/1 perhaps contributes to the salt tolerance of Nona Bokra by enabling high root K+ uptake under saline conditions. Other genes of the sub-family 2, OsHKT2;3 and OsHKT2;4 are structurally 93% similar at the amino acid sequence level and traceable on the reference rice genome of cv. Nipponbare (Horie et al. 2011a). They retain the four selectivity filter Gly residues typical of class II HKT transporters (Horie et al. 2009; Hauser and Horie 2010). Recently, OsHKT2;4 was shown to possess atypical Na+ transport properties and show dominant selectivity for K+ under competition over Mg2+ and Ca2+ ions, however, OsHKT2;3 failed to complement a high-affinity K+ uptake-deficient mutant of yeast strain (Horie et al. 2011a).

Other Genes for Salt Tolerance

Vacuolar sequestration by ion antiporters plays a significant role in maintaining osmotic balance in plants. Apart from these, several genes coding for osmotic homeostasis such as protein kinases, aquaporins and enzymes for osmolyte biosynthesis, enzymes for damage prevention and repair pathways such as antioxidant biosynthesis, Late Embryogenesis Abundant (LEA) proteins, dehydrins, antitoxic enzymes, chaperons, proteases, ubiquitination-related enzymes (Abogadalla 2010; Peleg et al. 2011), stress signaling pathways and a variety of transcription factors also regulate temporal and spatial gene expression. Polyamines (PA), the small aliphatic molecules positively charged at cellular pH, are modulated by salt stress and high PA levels have been positively correlated with stress tolerance (Alcázar et al. 2006; Kusano et al. 2008; Krasensky and Jonak 2012; Ahmad et al. 2012b). The induction of two OsLEA genes (OsLEA3, OsLEA21) by salinity has been clearly demonstrated through semi-quantitative RT-PCR analysis (Wang et al. 2007; Hu 2008). The membrane protein Na+/H+ antiporters catalyze the exchange of Na+ for H+ thereby helping plants to tolerate high salt levels through internal distribution of ions for osmotic adjustment and it has been shown that the expression of antiporter gene, OsNHX1 is increased in rice roots and shoots with salt stress (Fukuda et al. 2004). They further demonstrated that transgenic rice plants overexpressing the gene showed improved salt tolerance. Transcription Factors (TFs) defined as proteins which can activate or repress the gene expressions with its affinity for sequence specific DNA binding, has been shown to be involved in plant responses to stress including salinity. More than 40 TFs belonging to APETALA2/ethylene-responsive element binding proteins (AP2/EREBP), basic leucine zipper (bZIP), homeodomain proteins (HD), zinc finger proteins (ZFP), myeloblastosis (MYB), heteromeric CCAAT-box-binding heme-activator protein complex (CCAAT-HAP2), heat shock factor (HSF) and No apical meristem [NAM]-Arabidopsis Transcription Activation Factor [ATAF] - Cup shaped cotyledon [CUC] (NAC) gene families have been shown to be involved in rice responses to high salinity (Negrão et al. 2011). Three genes encoding ZFPs namely ZFP179, ZFP182 and SRZ1 have been reported as responsive to high salinity (Huang et al. 2007). The overexpression of ZFP179 (Sun et al. 2010) and ZFP182 and repression of SRZ1 improves salt tolerance (Huang et al. 2008a). Four genes encoding bZIPs (OSABF1, OsAB15, OsbZIP23 and OSBZ8) have been reported to be associated with salt stress responses (Hossain et al. 2010; Nakagawa et al. 1996; Xiang et al. 2008; Zou et al. 2008). Overexpression of OsbZIP23 improves salt tolerance while OSAB15 is a negative regulator of salt stress response and repression of this gene helps improving salt tolerance (Zou et al. 2008). TFs belonging to different families, such as MYB, HSF, Trihelix or CCAAT-HAP2 (OsMYB3R-2, OsGTγ -1 and OsHsfA2e) have also been found to be induced by high salinity and all improve salt tolerance (Dai et al. 2007; Fang et al. 2010; Liu et al. 2010a). More recently, Schimdt et al. (2012) showed that expression of an HSF, OsHsfC1b was induced by salt and overexpression of this gene improves salt tolerance in rice. One of the largest TF superfamily in plants is the NAC, which is known to play a significant role in abiotic stress tolerance in plants including salt tolerance. Rice has 151 NAC genes that are being shown to impart resistance to various stresses (Puranik et al. 2012).

Salt overly sensitive (SOS) pathway has been demonstrated to play a remarkable role in salt tolerance in Arabidopsis. A calcium signal elicited by salt stress is picked up by SOS3 protein and sends a downstream signal that activates SOS2, a serine/threonine protein kinase. SOS3 together with SOS2 regulate SOS1, a salt tolerance effector gene that encodes for a plasma membrane antiporter Na+/H+ (Yamamoto and Yano 2008). Rice has a conservative system of SOS pathway, with OsSOS1, OsSOS2/OsCBL4 and OsSOS3/OsCIPK24 showing functional similarity to their Arabidopsis counterparts AtSOS1, AtSOS2 and AtSOS3 (Martínez-Atienza et al. 2007; Kumar et al. 2012). Differential expression OsSOS2 has been established in salt tolerant (Pokkali) and sensitive (IR64) genotypes with tissue specific expression in field grown mature plants (Kumar et al. 2012).

Quantitative Trait Loci and Markers

Extending the DNA based molecular technology to classical linkage analysis, mapping of QTLs is the simplest way of identifying trait-related genomic regions that are otherwise difficult to identify due to several interfering factors such as polygenes, linkage, and low heritability. To date, several QTLs have been mapped for salt tolerance related traits in rice (Table 10.5), especially for the vegetative stage tolerance. Significant QTLs for reproductive stage tolerance are yet to be identified in rice (Jena and Mackill 2008). However, excepting few significant ones (Table 10.6) most of the QTLs identified so far are small effect QTLs and many of those reported from populations of early generations probably may remain in reports.
Table 10.5

Quantitative trait loci (QTLs) mapped for salt tolerance in rice

Cross

Population

No. of QTL

Method

Marker system

References

M20/77–170

F2

1

RFLP

Zhang et al. (1995)

IR29/Pokkali

RIL

10

IM

AFLP

Gregorio (1997)

Tesanai 2/CB

RIL

1

SF-ANOVA

RFLP

Lin et al. (1998)

M20/77–170

F2

1

SMA

RAPD

Ding et al. (1998)

Zhaiyeqing 8/Jingxi l7

DHL

8

SIM, CIM

RFLP

Gong et al. (1999)

IR64/Azucena

DHL

7

SIM

RFLP

Prasad et al. (2000)

IR 59462a

F7

16

AFLP

Flowers et al. (2000)

IR4630/IR15324

RIL

25

SMA

AFLP, RFLP, SSR

Koyama et al. (2001)

Zhaiyeqing 8/Jingxi l7

DHL

24

SIM

RFLP

Gong et al. (2001)

IR29/Pokkali

RIL

1

AFLP, SSLP

Bonilla et al. (2002)

Tesanai 2/CB

F8

31

SMA

RFLP

Masood et al. (2004)

Nipponbare/Kasalath

BIL

28

IM

RFLP

Takehisa et al. (2004)

Nona Bokra/Koshihikari

F3

8

SIM

RFLP

Lin et al. (2004)

IR64/ Tarom Molaii

BIL

??

CIM

SSR

Fotokian et al. (2005)

Milyang 23/Gihobyeo

RIL

3

IM

RFLP

Lee et al. (2007)

CSR 27/MI 48

F2

6

SIM

STMS

Ammar et al. (2007)

IR64/Binam

BIL

13–22

SIM

SSR

Zang et al. (2008)

AS996/IR50404

RIL

1

Regression

SSR

Lang et al. (2008)

Tarommahali/Khazar

F3

32

CIM

SSR

Sabouri and Sabouri (2008)

Tarommahali/Khazar

F2

14

CIM

SSR

Sabouri et al. (2009)

Tarommahali/Khazar

F3

12

CIM

SSR

Sabouri and Biabani (2009)

Ilpumbyeo/Moroberekan

BIL

8

CIM

SSR

Kim et al. (2009)

CSR 27/MI 48

RIL

18

CIM

SSR, SNP

Pandit et al. (2010)

IR29/Pokkali

RIL

17

CIM

SSR

Thomson et al. (2010)

Co39/Moroberekan

RIL

Many

IM

RFLP

Ul Haq et al. (2010)

IR26/Jiucaiqing

F9

16

MIM

SSR

Wang et al. (2011)

Tarome-Molaei/Tiqing

BIL

14

CIM

SSR

Ahmadi and Fotokian (2011)

Pokkali/IR29

BIL

13

SMA, Regression

SSR

Alam et al. (2011)

Pokkali/Shaheen Basmati

F3

22

SMA

SSR

Javed et al. (2011)

BRRI Dhan40/IR61920-3B-22-2-1

F2

3

SMA, CIM

SSR

Islam et al. (2011)

Teqing/Oryza rufipogon

IL

15

SMA

SSR

Tian et al. (2011)

aIR 59462  =  Nona Bokra/Pokkali//IR 4630-22-2-5-1-3/IR 10167-129-3-4

Table 10.6

Prominent quantitative trait loci mapped under salt tolerance screening

Trait

QTL

Chromosome

Flanking markers

R2 (%)

References

Salt tolerancea

Saltol

1

P3/M9-8 – P1/M-9-3

81.0

Gregorio (1997)

Seedling survival days

1

RG612 – C131

14.3

Gong et al. (1999)

Seedling root length

qSRTL-6

6

RG162 – RG653

18.9

Prasad et al. (2000)

Salt tolerance

Saltol

1

C52903S – C1733S

39.2

Bonilla et al. (2002)

Salt tolerance

Saltol

1

RM23 – RM140

43.2

Bonilla et al. (2002)

Salt tolerance

Saltol

1

CP03970 – CP06224

Niones (2004)

Shoot K+ concentration

qSKC-1

1

C1211-S2139

48.5

Lin et al. (2004)

Shoot Na+ concentration

qSNC-7

7

C1057-R2401

40.1

Lin et al. (2004)

Seedling salt tolerance

qST-1

1

Est12 – RZ569A

27.8

Lee et al. (2007)

Shoot Na–K ratio

qSNK1(Saltol)

1

RM1287 – RM10825

20.0

Thomson et al. (2010)

Imbibition rate

qIR-6

6

RM3687 – RM3306

33.6

Wang et al. (2011)

Imbibition rate

qIR-9

9

RM276 – RM5531

33.7

Wang et al. (2011)

Germination percentage

qGP-2

2

RM8254 – RM5804

36.5

Wang et al. (2011)

Germination percentage

qGP-9

9

RM219 – RM7048

43.7

Wang et al. (2011)

Relative root dry weight

qRDW-10

10

RM273

22.7

Tian et al. (2011)

Relative shoot dry weight

qRSW-10

10

RM273

17.3

Tian et al. (2011)

Relative total dry weight

qRTW-10

10

RM273

18.5

Tian et al. (2011)

aSalt tolerance  =  high K+ uptake  +  low Na+ uptake  +  low Na+/K+ ratio

Earliest attempt to map QTL for salt tolerance in rice was reported by Zhang et al. (1995), in which a QTL was mapped on chromosome 7 in an F2 population derived of the cross M-20  ×  77–170. M-20 was a stable mutant of 77–170 derived by in vitro selection. Later a large effect QTL was mapped on chromosome 1 in an IR29/Pokkali derived recombinant inbred line (RIL) population significantly influencing three salt tolerant traits viz., high K+ uptake, low Na+ uptake and low Na+/K+ ratio (Gregorio 1997). Named Saltol, this remains as the most prominent QTL mapped so far for salt tolerance in rice. Subsequently, two large effect QTLs were mapped for shoot concentration of Na+ and K+, qSNC-7 on chromosome 7 and qSKC-1 on chromosome 1, respectively in an F2:3 population between Nona Bokra, a salt tolerant indica landrace and Koshihikari (Lin et al. 2004), with qSNC-7 explaining 49% and qSKC-1 explaining 40% of the phenotypic variation. Later, qSKC-1 was cloned and found to encode a member of HKT-type transporters, OsHKT1;5, that is preferentially expressed in the parenchyma cells surrounding the xylem vessels. SKC1 protein functions as a Na+-selective transporter, involved in regulating K+/Na+ homeostasis under salt stress (Ren et al. 2005).

Map based cloning has become a useful tool in identifying genes that are responsible for the desired trait expression. It is now known that the best route forward to use a QTL is to identify it at the molecular level and to check their expression in each QTL combination. Developing of chromosome segment substitution lines (CSSLs) through backcross procedure will provide a route to accelerate this process (Yamamoto et al. 2009). Although a larger proportion of genes cloned by map-based cloning belongs to simple Mendelian traits, quantitative genes are also attempted to be cloned, with an objective of pyramiding genes targeting quantum improvement in the salt tolerance.

Recently a novel technique called MutMap-a method which combines DNA sequencing and EMS induced mutagenesis-has been developed for rapid gene isolation using a cross of the mutant to wild-type parental line (Abe et al. 2012). A mutant is crossed once with the wild type used for mutagenesis, followed by subsequent selfing. Gene identification is realized faster using MutMap with the help of next generation sequencing following the unequivocal segregation between the mutant and wild-type phenotypes. A programme for screening for salt tolerant genes from the cultivar Hitomebore has been initiated using MutMap, aiming at developing rice cultivars suitable for cultivation in the 2011 tsunami-hit of paddy fields of the Northern Japan coast (Abe et al. 2012).

Massive parallel sequencing of mRNA using RNA-Sequencing in Nipponbare has enabled the identification and annotation of genes which are differentially expressed under salt stress. Among the unannotated genes, 213 genes from shoot and 436 genes from root were differentially expressed in response to salinity stress (Mizuno et al. 2010).

The Saltol Region

The Saltol was mapped on the short arm of rice chromosome 1 derived from the tolerant parent Pokkali by AFLP genotyping (Gregorio 1997). The QTL had a LOD score of 14.5 and explained up to 81% of the phenotypic variation. Subsequently, Bonilla et al. (2002) integrated RFLP and SSR markers to the Saltol map, and in a hydroponic screen at the seedling stage using 54 RILs remapped this QTL that explained 43% of the phenotypic variation for shoot Na–K ratio. Further, many workers remapped and fine mapped Saltol in other mapping populations (Niones 2004; Lin et al. 2004; Elahi et al. 2004; Thomson et al. 2010). This QTL region is now confined within a 1.2 kb region (Niones 2004). Recent confirmative mapping of Saltol locus (Fig. 10.3), shows that Saltol contributes to Na+/K+ homeostasis with an LOD of 7.6 and R2 of 27% across the 140 RILs and a 30% decrease in the shoot Na–K ratio (Thomson et al. 2010). Saltol is flanked between microsatellite markers, RM1287 and RM7075 at physical position between 10.8 and 15.3 Mb on chromosome 1 (Alam et al. 2011).
Fig. 10.3

The Saltol region on chromosome 1 showing 18 polymorphic SSR markers, and peak of the QTL position for shoot Na/K ratio by simple interval mapping

SalT, another important gene, co-localized with Saltol on chromosome 1 was first isolated and characterized from the roots of salt-treated rice plants (Claes et al. 1990). Its expression is correlated with osmoprotectants, such as trehalose and ­proline. The treatment of rice with trehalose improved salt tolerance but suppressed SalT upregulation, while proline treatment increased growth inhibition of salt-treated rice plants and upregulated SalT (Garcia et al. 1997). SalT transcripts were found to accumulate with wounding and heat treatment and the gene is also induced by fungal elicitors, jasmonic acid and abscisic acid (de Souza et al. 2003; Kim et al. 2004; Moons et al. 1997), which suggests that the role of SalT protein may be involved in a broader response/ sensor mechanism to the imposed stress (de Souza et al. 2003).

FL478 (IR 66946-3R-178-1-1), a highly salt tolerant RIL otherwise similar to IR29 (Bonilla et al. 2002), was subsequently used as donor for salt tolerance breeding worldwide. Contrary to the expectations, investigations revealed that Saltol region of FL478 was indeed contributed by the sensitive parent IR29, but activated to trigger high salt tolerance in presence of other positive alleles form Pokkali (Walia et al. 2005). Saltol region of FL478 is very complex, and now poised to contain many Pokkali QTLs including that of SKC1 (Thomson et al. 2010) and a <1 Mb Pokkali DNA fragment at 10.6–11.5 Mb flanked by IR29 alleles (Kim et al. 2009). The fact that Saltol affected the Na–K ratio predominantly, the causal gene underlying this effect could be the sodium transporter SKC1 (OsHKT1;5) (Thomson et al. 2010).

Comparative genomic investigations reveal that Saltol region seemed to contain an array of homologous sequences of known genes, viz., transcription factors, signal transduction components, cell wall components, and membrane transporters (Walia et al. 2005, 2007). The membrane transporter genes included those coding for carriers and channels involved in transporting cations, anions and organic substrates such as sugar transporters (Senadheera et al. 2009). Specific genes identified so far are root tissue and membrane transporters such as cation-proton exchanger (OsCHX11) and Cyclic nucleotide-gated ion channel (OsCNGC1) (Senadheera et al. 2009), HKT1 (high affinity potassium transporter), ABC1 (ATP-binding cassette transporter) genes (Walia et al. 2005). Various other genes identified near Saltol are, salt stress-induced protein (EF576533) and tetracopeptide repeat domain containing protein (EF575991) showing salt induced activation (Kumari et al. 2009).

Improving Salt Tolerance in Rice

Cultivation of salt tolerant rice in India perhaps had begun much earlier than anywhere else in the world. Although there is no historical record available of its beginning, a traditional organic rice-shrimp farming system known as pokkali still exists in the coastal saline areas of Kerala that is characterized by daily ingression of tidal waves causing partial flooding of rice fields and seasonal shrimp farming in the rice fallows during high saline phase (Pillai 1999; Shylaraj and Sasidharan 2005). In fact, there were many pokkali rice varieties in use, all of which were salt tolerant. In India, however, organized research on breeding salt tolerant rice was begun circa 1940, especially in the states of Maharashtra and Madras. In 1943, two salt tolerant varieties Kala Rata 1–24 and Bhura Rata 4–10 were released in Maharashtra (Shendge et al. 1959). Around this time, in 1939, a salt-tolerant landrace called ‘Pokkali’ was introduced to Sri Lanka, which was later recommended for cultivation in saline areas in 1945 (Fernando 1949).

However, varietal development program for salt affected areas met with low success due to many reasons such as (a) lack of understanding of the complex nature of inheritance of salt tolerance, (b) lack of sufficient sources of resistance, (c) complexity and diversity of salt affected areas, (d) lack of precise and reliable screening techniques, and (e) lack of sufficient research backing. Conventional breeding methods such as introduction and selection of landraces, pedigree method, modified bulk pedigree method, mutation and shuttle breeding were used for development of new varieties in India (Reviewed by Singh et al. 2009). Shuttle breeding under an IRRI-India collaborative project had resulted in development of two salt-tolerant rice varieties, CSR23 and CSR27 (Mishra 1994).

Despite decade long breeding efforts, potential yield gap between the salt affected areas and normal regions remains wide, and there is an immediate need to harness resources to develop target-specific, locally adapted high-yielding varieties. Thanks to the modern approaches such as improved screening technique for phenotyping, in vitro and marker assisted selection, gap between potential and actual yield within these coastal areas is narrowing because of the development of salt-tolerant, fertilizer responsive and intermediate stature high-yielding varieties.

Screening for Salt Tolerance

Success of a target specific varietal development programme such as salt tolerance depends on reliable screening techniques that translates the results to reality in the field. Based on the target traits, methods of screening can be either phenological or physiological. While phenological screens included germination, survival, injury, morphology, yield and index such as mean tolerance index, physiological screening was done for Na+, K+, Cl concentrations and their derived ratios. Several screening techniques have been developed in rice such as hydroponics, pot culture, microplots and field evaluation, besides specialized solution culture screening methods such as bread boxes with perforated lids, seedling float technique and adult plant screening system (reviewed by Singh et al. 2010). Among all, field screening is the best because it is the only method that could accommodate salt tolerance in its holistic form with entire temporal and spatial variability. Notwithstanding, field screening is the most cumbersome of all the methods and hence limits the number of genotypes/ progenies to be handled per screening. However, augmented designs allow screening of large number of varieties than conventional complete designs. Artificially created soil plots that resembles mini in situ fields but devoid of soil heterogeneity and maintains gradient levels of salinity in each designated plots are used for microplot screening. Such microplots are utilized for screening early generation materials. For precise individual plant studies pot culture experiments are employed, which facilitate closer observations. Hydroponics screens have been very popular because of its simplicity in setting up, precise control over salt concentration and it helps in creating a water-plant interface to which rice is adapted. Furthermore, specialized laboratory screening such as prolonged soaking in high salt concentration for 9 days prior to germination test was proven to be effective in delineating salt tolerant varieties (Abeysiriwardena 2004). Salt tolerance at juvenile screening are classified based on a modified standard evaluation score (Gregorio et al. 1997) of visual salt injury at seedling level (Table 10.7).
Table 10.7

Salt tolerance classification based on the modified standard evaluation score of visual salt injury at seedling stage

Phenotype

Score

Tolerance

Normal growth, no leaf symptoms

1

Highly tolerant

Nearly normal growth, but leaf tips or few leaves whitish and rolled

3

Tolerant

Growth severely retarded; most leaves rolled; only a few are elongating

5

Moderately tolerant

Complete cessation of growth; most leaves dry; some plants dying

7

Susceptible

Almost all plants dead or dying

9

Highly susceptible

Most of these methods except field screening are limited to seedling stage, and therefore could not account for adult plant salt tolerance. Notwithstanding, artificial screens remain different from natural soil-water-plant interface limiting their direct application in crop improvement research. Therefore, an integrated approach is desirable that uses different screens so that the selected variety performs well under all stages of growth and therefore can be feasible for commercial cultivation.

In Vitro Techniques and Transgenesis

Since 1980s, cell and tissue culture techniques, have been recognized as powerful tools augmenting conventional breeding for the development of plants with increased tolerance to stresses such as salt stress. Later in vitro technology found their applications in molecular linkage mapping through Doubled Haploid (DH) lines and as an integral part of genetic engineering for the development of transgenic plants. In vitro techniques such as anther and pollen culture, somaclonal variation and protoplast fusion were used to develop salt tolerant lines in rice (Ram and Nabors 1985; Lynch et al. 1991). Among these, anther culture was used extensively in deriving salt tolerant lines, because of its advantage of faster development and efficiency in handling large number of progeny lines.

Anther Culture

The success of anther culture derived salt tolerant lines was established by the release of PSBRc50 (Bicol) targeted for saline-prone areas. Developed at IRRI, from the indica-indica cross IR5657-33-2/IR4630-22-2-5-1-3 (Zapata et al. 1991) this variety, originally known as IR51500-AC11-1, was the first ever anther culture derived variety to be released in the Philippines (Senadhira et al. 2002) and also the first cultivar recommended for adverse environments (Datta et al. 2009). Two other anther culture derived lines from IRRI, IR51500-AC17 and IR51485-AC6534-4 were released as commercial cultivars CSR21 and CSR28, respectively, for cultivation in saline-alkaline soils of India. Several anther derived DH lines were developed at IRRI, most of which had been used as a donor parents in breeding programs in various rice growing nations (Datta et al. 2009).

Although anther culture has limitations of reduced success, anther derived lines are still being developed for salt tolerance. Recently in Bangladesh, Rahman et al. (2010) generated 25 salt tolerant DH lines from a cross IR52724/ BR36 with line AC 1 showing excellent seedling stress survival coupled with moderately low Na/K ratio close to that of the tolerant control Pokkali, besides producing good yield in field trials conducted in a saline zone. Similarly many anther derived lines are under testing in Vietnam (Tam and Lang 2004) and Thailand (Cha-um et al. 2008).

Somaclonal Variation

Successful exploitation of somaclonal variants, the mutant cell lines that survive in salt rich selective media and regeneration of whole plants from such variants, stimulated many attempts for the development of salt-tolerant plants (Reddy and Vaidyanath 1986; Kavi-Kishor 1988). Although several salt tolerant lines have been reported, in many cases regenerants either failed to inherit the trait effectively, or showed developmental defects or in extreme cases showed complete reversal of tolerance. Such failure are now attributed to lack of distinction between mutant and adapted cell lines, distinct driving mechanisms for cellular and whole plant tolerance, multigenicity of salt tolerance and loss of regeneration capacity during selection (Tal 1993; Oono 1984). In an earlier reported attempt from IRRI, Pokkali cell lines were subjected to in vitro induction of somaclonal variants, with the objective of improving agronomic traits. A variant, TCCP 266-2-49-B-B-3 had improved agronomic performance coupled with good salt tolerance (Senadhira et al. 1994), showing vigorous growth, semi-dwarf nature, white pericarp and better cooked rice quality, features that were distinctly different from the original Pokkali line, which was tall with red pericarp and poor cooking quality. TCCP266-2-49-B-B-3 has later become a popular donor for producing new high-yielding salt-tolerant lines, some of which were released as varieties (Datta et al. 2009).

Transgenesis

Development of transgenic plants, by introducing new genes from external sources is an ideal tool to test the expression of orthologous genes. With the advancement in molecular mapping of QTLs together with transcriptome and whole genome profiles, map-based cloning has been successfully used to isolate and clone candidate genes and QTLs of biological and/or agricultural importance (Senadheera et al. 2009). However, before putting them into use it is essential to functionally validate the genes for trait expression. This helps to target the gene precisely and develop markers for marker assisted selection (MAS) programmes. In the modern biology, information on useful genes accumulate from different directions such as whole-genome information of both eukaryotic and prokaryotic model organisms, expressed sequence tag (EST) libraries, QTL mapping, microarrays etc. and transgenic system is the most handy tool in testing the expression of target genes under given environments such as high salinity. The testing can either be on the same or different organisms.

Several rice genes have already been positively tested in plant systems such as Arabidopsis, maize, tobacco and within rice itself, besides testing of foreign genes in rice for their role in imparting salt tolerance through transgenic approaches (Tables 10.2 and 10.3). In many cases Agrobacterium mediated gene transfer has been used to generate transgenic plants, proving the usefulness of transgenic approach in gene validation.

Molecular Breeding

With the availability of several molecular markers and saturated molecular genetic map of rice, MAS has now become feasible both for traits controlled by major genes as well as QTLs. Molecular breeding, a generic term now includes different MAS approaches, such as marker assisted backcrossing (MABC), marker assisted recurrent selection (MARS) and MAS based diallel selective mating system (MAS-DSMS). MAS has two distinct advantages translating to significant monetary and time benefits, namely, (a) it reduces the product delivery time considerably and (b) it reduces the genetic load or linkage drag associated commonly with backcross breeding programmes (Alpuerto et al. 2008; Gopalakrishnan et al. 2008; Singh et al. 2012). Furthermore, it is now possible to defer early generation phenotyping of segregating populations, by foreground selecting for stable QTLs and genes that have already been validated to confer stable salt tolerance under varying situations. This can accelerate breeding cycle as well as helps in handling large number of individuals per population, channeling to a successful salt tolerant variety. MAS as a tool to augment breeding programme, is widely used in targeted transfer of specific genes/ QTLs into popular cultivars through indirect selection based on gene or QTL linked based markers for foreground selection (Singh et al. 2011).

Marker Assisted Backcrossing

MABC is of great practical interest in applied breeding programmes, because it is done almost in the conventional way, but without or minimized phenotype testing in the early generations, rapidly advancing to the target genotype by following the inheritance of simple molecular tags that segregate in classical Mendelian fashion. Given the information available, molecular markers can be successfully deployed for foreground as well as background selection in order to confirm the presence of resistance gene(s) and speedy recovery of recurrent parent genome (RPG) and phenome (Singh et al. 2011). Detailed reviews on usefulness of MABC in rice are now available (Collard and Mackill 2008; Singh et al. 2011).

MABC for transferring salt tolerance QTL, Saltol is currently practiced in many rice growing nations, viz., Philippines, India, Thailand, Vietnam and Bangladesh (Elahi et al. 2004; Singh et al. 2011; Lang et al. 2011). The procedure involves crossing of the Saltol donor (preferably FL478) with the recipient in three backcrosses, selecting for the markers flanking the Saltol (foreground selection) and selecting against the donor markers for other regions (background selection) within each backcross generations. At the end of the programme recombinants are selected in which Saltol alleles are fixed, and show salt tolerance as against the original recipient. Various MABC procedures are in practice that combines phenotype selection for faster background recovery (Singh et al. 2011), together with stepwise transfer or simultaneous transfer or simultaneous and stepwise transfer for QTL pyramiding (Joshi and Nayak 2010).

In India, FL478 is being used as a donor to transfer Saltol into the recurrent parents Pusa Basmati 1121 and Pusa Basmati 6 through MABC in two independent backcross programs. Three Saltol linked markers RM8094, RM3412 and RM493 that are polymorphic between the recurrent and donor parents are used for foreground selection in each backcross generation, coupled with stringent phenotypic selection for rapid recovery of RPG and phenome with salt tolerance (Singh et al. 2011; Babu et al. 2012). Furthermore, various institutions across India are working on transferring Saltol in the backgrounds of popular rice varieties such as Sarjoo 52, Pusa 44, PR114, Gayatri, Savithri, MTU 1010, White Ponni and ADT45. IRRI in collaboration with national institutes under Stress-Tolerant Rice for Africa and South Asia (STRASA) project is gearing up with MABC for transferring Saltol into popular varieties such as BRRI dhan 28, IR64, BR11 and Swarna (STRASA 2011).

Marker Assisted Recurrent Selection and Diallel Selective Mating System

MARS and its variant DSMS-MAS are recent introductions in molecular breeding protocols and are not widely being practiced. MARS targets the identification and selection of several genomic regions involved in the expression of complex traits to ‘assemble’ the best-performing genotype within a single, or across related populations (Ribaut et al. 2010), while DSMS-MAS uses a multi-parent crossing strategy to develop recombinants using partial or full diallel crossings and select those recombinants with desired alleles and employ them into intensive crossing programmes so that the ultimate genotypes accumulate as many desired genes as possible so the probability of selection of desired combinations become maximized (Singh et al. 2010). These methods, although long term, has the advantage of transferring multiple stress resistance, are gaining importance as permanent breeding strategy in institutes like IRRI. Selection for Saltol is now routinely done at IRRI for selection of desirable recombinants for selective mating (Singh et al. 2008; Gautam et al. 2009).

Association Mapping and Genomic Selection

Association mapping (AM) and genomic selection (GS) are latest technologies that have found applications in plant molecular breeding (Abdurakhmonov and Abdukarimov 2008; Heffner et al. 2009). Although both differ in their applications, these techniques promise identification and use of target genomic regions that are otherwise difficult to map using QTL mapping approach. Both these techniques use more accurate and ubiquitous single nucleotide polymorphisms (SNPs) and genome wide variations. AM is based on the evolutionary linkage disequilibrium, that is conserved in the haplotype blocks and identification of the precise marker-trait association on an unstructured population, providing better precision of the associated markers to the target trait. Emerging scientific reports indicate that many laboratories are currently working on AM towards identifying novel QTLs associated with salt tolerance in rice (Courtios et al. 2011; Li et al. 2012). AM in the European rice core collection (ERCC) has recently identified 19 distinct loci associated with salt tolerant traits in the temperate japonica background, divulging that no accession carried all favorable alleles suggesting the potential for further improvement. The effective strategy for the accumulation of the favorable alleles would be marker-assisted population improvement (Ahmadi et al. 2011).

Rapid advances in the development of novel high-throughput DNA sequencing has drastically reduced the cost of whole genome sequencing, providing low cost coverage of any genome. Whole genome sequence resources are useful in the development of high density molecular markers that could be used in molecular marker assisted breeding (Subbaiyan et al. 2012). Genomic selection (GS) is the selection based on genomic estimated breeding value (GEBV) determined from simultaneous estimation of all locus effects across the genome in a set of training population without significance testing and without identifying a priori a subset of markers associated with the trait (Heffner et al. 2009). GS is gaining popularity in molecular breeding because it eliminates the need of QTL mapping and provides renewed promise in breeding for difficult traits such as salt tolerance. GS is still at the exploratory stage for plants, however, many laboratories have already started using the technique in rice, and one of the target traits set is salt tolerance.

Achievements, Impact, and Prospects

Breeding for salt tolerance in rice has taken a leap forward during last 15 years. In India, remarkable progress was achieved in developing improved salt tolerant genotypes at the CSSRI under the IRRI-India collaborative project. So far nine varieties (CSR21 to CSR29) were developed under this project and recommended for cultivation at various salt-affected ecologies (Singh et al. 2009). MABC derived IRRI-bred salt tolerant variety carrying Saltol, IR63307-4B-4-3, has been recently released in Bangladesh as BRRI dhan47 (Salam et al. 2007), and in the Philippines for cultivation. Many popular varieties are in the pipeline of MABC based improvement. Reason for the success of these programmes can be attributed to the practicable developments in the molecular biology together with better phenotyping screens augmented with tremendous developments in computing, communication and automation. Although conventional breeding efforts for the past 70 years had amassed wealth of information on salt tolerance behavior in rice, in addition, today we know more about the intricate mechanisms of salt stress signaling and responses in plants. The novel information in tandem with the age-old wisdom can now be channelized towards precise development of novel rice cultivars with improved tolerance.

For having promoted for better performance than the existing stock on a contemporary scale, majority of the rice varieties developed through conventional approaches worldwide have varying levels of salt tolerance. Many of them are low to medium yielders with poor quality grains. The present day understanding of the genetics of various agronomic traits and salt tolerance can steer molecular breeding towards an integrated crop improvement approach for high yielding good quality salt tolerant rice genotypes in the future.

Several reports that are available on screening of germplasm for salt tolerance, like that of screening of more than 25,000 rice germplasm at IRRI identifying 1,495 salt tolerant types with varying levels of tolerance (Ponnamperuma and Bandyopadhya 1980) and similar efforts in other countries indicate that massive breeding efforts are required to bring together desired genes into limelight. Notwithstanding, the key to success lies in the unexplored germplasm, especially in the landraces, that were traditionally grown in saline lowlands. Excepting Pokkali and Nona Bokra, not many traditional saline tolerant varieties have been subjected to serious investigations. In India, besides pokkali rice types there are several salt tolerant rice varieties that remains to studied in detail, such as Assgo, Bello, Damgo, Kalo Damgo, Kalo Korgut, Kalo Novan, Khochro, Korgut, Muno and Shiedi from the khazan lands of Goa (Bhonsle and Krishnan 2011). It is unlikely that all the traditional salt tolerant varieties would be harboring variants of the major QTL, Saltol. Having long term programmes aimed at allele mining from salt tolerant rice germplasm, mapping QTLs, cloning of tolerance QTLs/genes, pyramiding of multiple genes and QTLs coupled with yield and quality would be the ideal strategic solution for developing varieties suited for saline environments. Recent developments of AM, GS and high throughput techniques such as MutMap (Abe et al. 2012), are promise towards future for novel gene mapping and allele mining technologies (Henry et al. 2012).

Recent developments in salt tolerance research with accomplishments on the discovery of several functional genes and QTLs is poised to take new challenges for the future. Soon the MAS attempts will reflect in significant improvements in tolerance of salt-sensitive varieties.

Conclusion and Future Perspective

Growing concerns of land salinization is threatening crop productivity in major rice growing areas of the world. The issue is more serious because rice, the crop that feeds half the world, is sensitive to salinity. Varying sensitivity at different phenological stages of crop growth, particularly the high sensitivity during seedling and flowering stages strongly compromises plant survival and yield. With the world population growing incessantly, there is an urgent need to produce more grains from the salinized lands as well as to reutilize lands that are rendered unproductive due to salt accumulation. Although variability exists in rice germplasm towards salt tolerance, conventional breeding has been far less fruitful in addressing this complex problem. Probable reasons are lesser understanding of the nature of salt tolerance genetics, poorer screening facilities, biased screening towards juvenile tolerance, poor exploitation of the germplasm and lack of integrated breeding approaches towards an ‘ideal’ cultivar. It is essential to develop varieties that are phenologically capable of sustaining excess salt throughout its life span and produce higher yield and better quality. With the deeper understanding of the intricate mechanisms of salt tolerance and the array of genes and useable QTLs that are being discovered every day, the breeding scenario towards salt tolerant rice is poised to take a more productive turn in near future. Since QTLs are measurable and identifiable in the genome, it is essential to identify the genes underlying the trait so that genetic load or linkage drag from the undesirable genes can be minimized. Association mapping and genome wide selections are already making their footprints in salt tolerance research in rice. Complimentary validation of candidate genes using transgenic and transcriptomic approaches are supplementary tools in designing precise MAS strategies. Since MAS is going to be an integral part of the future breeding plans, it should be made much simpler so that breeders can perform the selection using a minimum genotype screening setup, which will boost the success of participatory and shuttle breeding approaches that promise sustainable cultivars for the future.

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Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • K. K. Vinod
    • 1
  • S. Gopala Krishnan
    • 2
  • N. Naresh Babu
    • 2
  • M. Nagarajan
    • 1
  • A. K. Singh
    • 2
  1. 1.Division of Genetics, Rice Breeding and Genetics Research CenterIndian Agricultural Research InstituteAduthuraiIndia
  2. 2.Division of GeneticsIndian Agricultural Research InstituteNew DelhiIndia

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