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agronomy Review Bridging the Rice Yield Gaps under Drought: QTLs, Genes, and Their Use in Breeding Programs Nitika Sandhu and Arvind Kumar * International Rice Research Institute, DAPO BOX 7777, Metro Manila 1301, Philippines; n.sandhu@irri.org * Correspondence: a.kumar@irri.org; Tel.: +63-2-580-5600 (ext. 2586) Academic Editor: Silvio Salvi Received: 5 January 2017; Accepted: 27 March 2017; Published: 9 April 2017 Abstract: Rice is the staple food for more than half of the world’s population. Although rice production has doubled in the last 30 years as a result of the development of high-yield, widely adaptable, resource-responsive, semi-dwarf varieties, the threat of a food crisis remains as severe as it was 60 years ago due to the ever-increasing population, water scarcity, labor scarcity, shifting climatic conditions, pest/diseases, loss of productive land to housing, industries, rising sea levels, increasing incidences of drought, flood, urbanization, soil erosion, reduction in soil nutrient status, and environmental issues associated with high-input agriculture. Among these, drought is predicted to be the most severe stress that reduces rice yield. Systematic research on drought over the last 10 years has been conducted across institutes on physiology, breeding, molecular genetics, biotechnology, and cellular and molecular biology. This has provided a better understanding of plant drought mechanisms and has helped scientists to devise better strategies to reduce rice yield losses under drought stress. These include the identification of quantitative trait loci (QTLs) for grain yield under drought as well as many agronomically important traits related to drought tolerance, marker-assisted pyramiding of genetic regions that increase yield under drought, development of efficient techniques for genetic transformation, complete sequencing and annotation of rice genomes, and synteny studies of rice and other cereal genomes. Conventional and marker-assisted breeding rice lines containing useful introgressed genes or loci have been field tested and released as varieties. Still, there is a long way to go towards developing drought-tolerant rice varieties by exploiting existing genetic diversity, identifying superior alleles for drought tolerance, understanding interactions among alleles for drought tolerance and their interaction with genetic backgrounds, and pyramiding the best combination of alleles. Keywords: drought; marker; pyramiding; QTLs; rice; genomics 1. Introduction Rice feeds more than half of the global population. Global rice (paddy) production in 2015 trails 0.8 percent behind the 2014 outcome, 738.2 million tons (490.3 million tons, milled rice), obtained from an area of 160.6 million hectares, a decrease of 1.3% [1]. Asia, where 60% of the earth’s population lives, is the major producer and consumer of the world’s rice. Water, climate, season, rainfall, soil conditions, agriculture inputs, and genetic potential of germplasm are key determinants of crop productivity. Increasing population (Figure 1a), increasing demand for water (Figure 1b), water crisis (Figure 1c), drought (Figure 1d), failure to adapt to climate change, declining farm land, soil moisture, soil characteristics, deterioration in nutrient content, weed competitiveness, increasing intensity, and the frequency of biotic/abiotic stresses will amplify the challenges of achieving future food requirements. This will affect the economic growth and social stability of regions with food shortages. Farmers will earn a profit only if they successfully solve the algebraic puzzle of farming. Wheat, rice, maize, and Agronomy 2017, 7, 27; doi:10.3390/agronomy7020027 www.mdpi.com/journal/agronomy Agronomy 2017, 7, 27 2 of 27 Agronomy 2017, 7, 27 2 of 26 other grains that are the staple food of the human population and the sources of feed for livestock account more for thanlivestock 60% of the total crop evapotranspiration requirement, soybeans and sources for of feed account for more than 60% of the total cropwhile evapotranspiration other oilseed crops forand 17%, and oilseed sugarcane 6%account [2]. In such circumstances, the available requirement, whileaccount soybeans other crops for 17%, and sugarcane 6% [2]. Inwater such resources will not be sufficient to produce enough food for the increasing population. With changes in circumstances, the available water resources will not be sufficient to produce enough food for the the climate and unpredictable rainfall, there is a possibility that nearly half of the world’s population increasing population. With changes in the climate and unpredictable rainfall, there is a possibility may water by 2030 population [3]. Water scarcity willwater worsen in theby world’s extremely dry regions that face nearly halfscarcity of the world’s may face scarcity 2030 [3]. Water scarcity will and areas where water is already in short supply. worsen in the world’s extremely dry regions and areas where water is already in short supply. Figure1.1.(a)(a) Projected population (source: U.S. Bureau, Census International Bureau, International database Figure Projected population curvecurve (source: U.S. Census database 1950–2050, 1950–2050, July 2015 estimated water demand (OECD: Organization Economic July 2015 update); (b) update); estimated(b) global waterglobal demand (OECD: Organization for Economicfor Cooperation Cooperation and Development; BRIC: Brazil, Russia, India andRest China; RoW: source: Rest of United world; Nation source: and Development; BRIC: Brazil, Russia, India and China; RoW: of world; United Food Organization); & Agriculture Organization); (c) severity pattern stress country by Food & Nation Agriculture (c) severity pattern of water stressofbywater country byby 2040 (source: 2040 (source: World Resource Institute); (d) estimated possibilities for future drought worldwide World Resource Institute); (d) estimated possibilities for future drought worldwide based on the based on the Palmer Drought Severity Aigup Index Dai, (source: Aigup Dai, Wiley interdisciplinary Palmer Drought Severity Index (source: Wiley interdisciplinary Reviews: ClimateReviews: Change, July 2012). Climate Change, July 2012). The contribution contributionofofplant plant breeding to improving commercially important including The breeding to improving commercially important crops,crops, including major major ones such as rice, maize, wheat, cotton, and pearl millet, at a global level is remarkable. Before ones such as rice, maize, wheat, cotton, and pearl millet, at a global level is remarkable. Before the the Green Revolution, traditional and wheatwere varieties were tall, photoperiod-sensitive, Green Revolution, traditional rice andrice wheat varieties tall, photoperiod-sensitive, low-yielding low-yielding and drought-tolerant, having a broad maturity duration andquality. good grain quality. In the and drought-tolerant, having a broad maturity duration and good grain In the post-Green post-Greenera, Revolution era, these traditional varietiesby were by a few widelyincluding adapted Revolution these traditional varieties were replaced a fewreplaced widely adapted varieties varieties including inbreds and hybrids that are dwarf and photoperiod-insensitive, with early inbreds and hybrids that are dwarf and photoperiod-insensitive, with early maturity, higher yield, maturity, poor grain quality,The anddwarf low pest resistance. Thebred dwarf rice varieties were poor grain higher quality,yield, and low pest resistance. rice varieties were by targeting irrigated bred by targeting irrigated ecosystems wherein ample water was thought to remain available for ecosystems wherein ample water was thought to remain available for traditional practices of puddled traditional practices of puddled transplanted system of rice cultivation. These varieties have high transplanted system of rice cultivation. These varieties have high yield potential and good resistance yield potential resistance to biotic stresses, but are highly susceptible abiotic stresses to biotic stresses,and but good are highly susceptible to abiotic stresses such as drought. Theytoare also prone to such as drought. They are also prone to heavy yield losses even under mild drought stress [4]. In the course of post-Green Revolution breeding over the past 50 years, unknowingly, the drought tolerance contributing alleles of traditional cultivars have not been properly maintained in the Agronomy 2017, 7, 27 3 of 27 heavy yield losses even under mild drought stress [4]. In the course of post-Green Revolution breeding over the past 50 years, unknowingly, the drought tolerance contributing alleles of traditional cultivars have not been properly maintained in the modern cultivars. Recent understanding of molecular and physiological mechanisms for different abiotic stresses has opened up new opportunities to improve yield under adverse climatic conditions for many crops. There is still a need to bridge the large gap between yields in most favorable and stress conditions. Strategies involving bridging the yield gap and increasing yield stability and adaptability under variable environmental conditions are of importance in assuring food security and sustainability in the future. There is a need to move forward from the Green Revolution to a ‘gene revolution,’ which is more productive and more ‘green’ in terms of conserving natural resources and the environment [5]. 2. Drought: The Key Concern in Food Security Drought has been the main catalyst of many large famines of the past and has a major destructive effect on rice production in rainfed areas across Asia and sub-Saharan Africa. The most vulnerable, drought-prone areas are shown in Table 1. The most devastating drought events around the world were the Deccan Famine and those in the Horn of Africa, the United States, Vietnam, Australia, China, Brazil, the Sahel, Malawi, East Africa, Ethiopia, India, and Bangladesh. From 2003 to 2013, at least one medium- to large-scale natural disaster caused $70 billion in crop and livestock production losses; drought alone accounted for 44%. Asia is the most affected region, with total crop and livestock production losses amounting to $28 billion (40% of total losses), followed by Africa with $25 billion (Table 2) [6]. The 1987 drought in India, the 2004 drought in Thailand, and the 1978–2003 drought in China were estimated to have affected 60% [7], 2 million ha [8], and 14 million ha of cropped area, respectively. Drought events between 1980 and 2014 in sub-Saharan Africa affected 203, 86, 74, 61, and 48 million people in eastern Africa, southern Africa, western Africa, Ethiopia, and Kenya, respectively [6]. Table 1. Most vulnerable drought-prone areas across the world. Region Areas Most Vulnerable to Drought Drought Events Asia/Pacific India, Nepal, Bangladesh, China, Laos, Cambodia, Pakistan, Afghanistan, Sri Lanka, Bhutan, Indonesia, Thailand, Myanmar, Vietnam, Malaysia 1876, 1878, 1896, 1902, 1907, 1928, 1930, 1936, 1941, 1942, 1944, 1958, 1961, 1964, 1972, 1973, 1974, 1983, 1987, 1993, 1996, 2000, 2002, 2010 Middle East Yemen, the United Arab Emirates, Saudi Arabia, Iraq, Iran, Syria 1940, 1998, 2000, 2007, 2010 France, Italy, Germany, northern Spain, Czech Republic 1955, 1957, 1962, 1968, 1971, 1974, 2005, 2009, 2012 Arizona, Kansas, Arkansas, Georgia, Florida, Mississippi, Alabama, South, North Carolina, Texas, Oklahoma, California 1934, 1936, 1939, 1940, 1983, 2002, 2010, 2011 Ethiopia, Kenya, Eritrea, Somalia, Uganda, Djibouti, Mauritania, Angola, Zambia, Zimbabwe, Mozambique, Malawi, Lesotho, Swaziland 1888, 1972, 1973, 1983, 1985, 1991, 1992, 1999, 2002, 2002, 2003, 2010, 2011, 2012 Peru, Chile, Argentina, Brazil, Mexico 1630, 1640, 1650, 1782, 1884, 1992, 1999, 2011, 2015 New south wales, Queensland, Victoria, Tasmania, Sydney, Northam, York area of Western Australia 1813, 1826, 1829, 1835, 1838, 1850, 1888, 1897, 1902, 1982, 1983, 2000 Europe United States Africa Latin America Australia Source: Modified from Spring 2015 global attributes survey. Agronomy 2017, 7, 27 4 of 27 Table 2. Effect of drought on crops and livestock across the world. Region Crop Losses (Billion USD) Livestock Losses (Billion USD) Total (Billion USD) Africa Asia Latin America and Caribbean Near East Central Asia % share of total Global losses 21 27 9 4 1 42.4 4 1 2 0 0 35.8 25 28 11 4 4 78.2 Source: FAO based on data from FAOSTAT, 2003–2013. Drought induces critical losses in crop yield. Yield integrates many of the physiological and biochemical responses at cellular and molecular levels, influenced by a number of predictable and unpredictable factors that are genetically difficult to understand and manipulate. Therefore, long-term and systematic attention should be given to the complex issues surrounding drought in order to develop a better understanding and devise sustainable solutions. 3. Effect of Drought on Different Crops Approximately 34% of rice is grown in rainfed lowland, 9% in rainfed upland, and 7% in flood-prone areas, while irrigated ecosystem covers 50% of total world rice area. Drought has been reported to produce devastating effects in rice at panicle initiation and flowering [4,9]; in maize at the tasseling and silking stages [10,11]; in sorghum and pearl millet at the booting and flowering stages [12]; in finger millet at the flowering stage; in sunflowers at head formation and the early grain-filling stage [13,14]; in groundnuts at the peg penetration and pod development stages; in soybean at the flowering and pod filling stages [15,16]; in black and green gram at the flowering and early pod development stages [17]; in cotton at the square formation and ball development stages [18,19]; and during the reproductive stage in rice [20,21]. Like in other crops, in rice drought has the most devastating effect at the reproductive stage. In rice, the damage to the crop is also significant at the seedling as well as vegetative stages. At the seedling stage, delay in monsoon rains, insufficient rain to puddle land, and preparation for transplanting force farmers to leave their land uncultivated. Severe drought at the vegetative stage reduces biomass production, causes the death of the plant and in severe cases, forces farmers to allow the grazing of the crops by cattle. Drought has a complex effect on plants [22–42], and plants respond with many defensive adaptations (Figure 2). The major determinants of grain yield under drought are the variety [43], type of soil [44], length and timing of drought [45], severity of drought [46,47], season (early season, mid-season, or terminal stage, Table 3 [48–68]), the age, period, and development stage of the plant [69], plant responses after stress elimination, and the interaction between the biotic/abiotic factors [70] and the region. Apart from this, drought stress also makes the rice crop more susceptible to biotic stresses (rice blast, brown spot, and bacterial blight), leading to a further decline in rice production. In many rice-growing areas in rainfed ecosystems, drought and submergence can occur in the same season at different growth stages of the plant or in different seasons, thus creating more complexity. Drought tolerance is a means for the rice plant to survive and produce a stable and satisfactory yield. There is urgent need for a strategy to get the highest yield out of every single drop of water on existing cropland to satisfy food needs in the future. Agronomy 2017, 7, 27 5 of 27 Table 3. Yield losses in different crops as a result of drought. Crop Rice Rice Rice Rice Rice Wheat Pearl Millet Pearl Millet Agronomy 7, 27 Pearl2017, Millet Maize Barley Barley Chickpea Chickpea Chickpea Chickpea Pigeon Pea Pigeon Pea Canola Canola Stress Lowland moderate reproductive stage Lowland severe reproductive stage Upland mild reproductive stage Upland moderate reproductive stage Upland severe reproductive stage Moderate reproductive stage Prior and beginning of flowering Early stress Late stress Mild-moderate-severe reproductive stage Severereproductive reproductivestage stage Severe Late terminal drought Late terminal drought Reproductivestage stage Reproductive Reproductive stage Reproductive stage Reproductive stage Reproductive stage Yield Reduction 45%–60% 65%–91% 18%–39% 70%–75% 80%–97% 10%–50% 65% 62% 28% 1%–76% 73%–87% 73%–87% 49%–54% 49%–54% 45%–69% 45%–69% 40%–55% 40%–55% 15%–35% 15%–35% Reference [48–50] [48–51] [48,52] [48,52] [48,49,53] [54–57] [58] [59] 5 of 26 [59] [60–63] [64] [64] [65] [65] [66] [66] [67] [67] [68] [68] Figure 2. Effect of drought and approaches in developing drought-tolerant rice varieties. RILs: Figure 2. Effect of drought and approaches in developing drought-tolerant rice varieties. RILs: Recombinant inbred lines, NILs: Near-isogenic lines, DH: Double haploid, NGO: Non-Governmental Recombinant inbred lines, NILs: Near-isogenic lines, DH: Double haploid, NGO: Non-Governmental Organization; IYT: Intermediate Yield Trial, PYTs: Preliminary yield trial, ↑ (increase/enhance), ↓ Organization; IYT: Intermediate Yield Trial, PYTs: Preliminary yield trial, ↑ (increase/enhance), ↓ (decrease/reduce). (decrease/reduce). Water availability (drought and flood), soil problems (salinity, nutrient deficiencies, and toxicities), extreme temperatures andsoil cold) and biotic stresses nutrient (brown planthopper, Water availability (drought and(heat flood), problems (salinity, deficiencies,gall andmidge, toxicities), blast, tungro, bacterial blight) are the main constraints in South Asia, Southeast Asia, and Africa, extreme temperatures (heat and cold) and biotic stresses (brown planthopper, gall midge, blast, tungro, where rice often suffers from extensive shock to sustain full yield potential. Surveys conducted by bacterial blight) are the main constraints in South Asia, Southeast Asia, and Africa, where rice often the Africa Rice Center in 12 sub-Saharan African countries reported a yield decline of 33% [71] when suffers from extensive shock to sustain full yield potential. Surveys conducted by the Africa Rice Center drought and flooding occurred together. Another study by the Africa Rice Center reported yield in 12 losses sub-Saharan African a yield decline of 33% [71] when and [72]. flooding of 40% and 25% countries in Senegal reported and Uganda, respectively, due to salinity anddrought iron toxicity occurred together. Another study by the Africa Rice Center reported yield losses of 40% and 25% in Therefore, it is advantageous to select cultivars with multiple stress tolerance (drought, salinity, Senegal and Uganda, respectively, to salinity andhigh irontemperature) toxicity [72].toTherefore, it is advantageous to submergence, stagnant flooding,due biotic stress, and allow the crop to survive if multiple stresses come at the same time. 4. Strategies to Manage Drought Comprehensive information, early warning systems and cultivation of high-yielding, high-quality, drought- plus biotic stress-tolerant varieties in drought-prone areas could provide a Agronomy 2017, 7, 27 6 of 27 select cultivars with multiple stress tolerance (drought, salinity, submergence, stagnant flooding, biotic stress, and high temperature) to allow the crop to survive if multiple stresses come at the same time. 4. Strategies to Manage Drought Comprehensive information, early warning systems and cultivation of high-yielding, high-quality, drought- plus biotic stress-tolerant varieties in drought-prone areas could provide a solution to the problem of drought. Identification and introduction of suitable traits that narrow the gap between expected and actual yield; understanding realistic physio-morpho-molecular mechanisms of drought tolerance; and designing a standard screening method for a large population [73] could contribute to the development of drought-tolerant rice varieties. Adopting proper strategies such as larger scale standardized screening for grain yield under drought and understanding the components of yield based on morpho-physiological traits could contribute to breeders’ efforts to develop better drought-tolerant varieties. Conventional and marker-assisted breeding strategies based on the use of drought-tolerant donors, pre-breeding to use the lines derived from crosses involving donors, and the development of suitable mapping populations to identify QTLs/genes affecting yield could result in yield improvement and stability under drought stress. Breaking undesirable linkages between drought tolerance and tall plant height, drought tolerance and earliness, and drought tolerance and low yield potential [74] could help to develop semi-dwarf drought-tolerant varieties without any yield penalty. Molecular, cellular, physiological, biochemical, and developmental responses to abiotic stress involve several genes and gene functions controlling drought tolerance. Several efforts have been made to better understand the expression of drought-tolerance-related traits and the complex network of drought-related genes. Exogenous application of hormones and osmoprotectants to seed or growing plants, engineering for drought resistance, and high-throughput novel technologies could be useful tools in identifying genes to improve yield under drought (Figure 2). 4.1. Screening Strategies Although it is difficult to understand how plants build up, combine, and exhibit the changing processes over the entire growth and development cycle, efforts have been made to standardize screening protocols, understand the mechanisms related to drought tolerance, and develop varieties that are tolerant of drought. The assessment of the type, intensity, degree of drought, and appropriate selection/screening for drought tolerance is a very crucial step. Each method has some advantage and limitations. Identification of drought-tolerant and -susceptible cultivars based on a few physiological measures (such as canopy temperature, water potential, and osmotic adjustment) [75] and specific environmental factors (such as weather and soil water availability) may not be adequate for breeders to use such donors in the breeding program. Screening of donor lines for grain yield under drought, performance of such lines under both stress and non-stress conditions [76–79], and use of robust statistical methods to clearly differentiate drought-tolerant and drought-susceptible lines [80–83] could be considered an appropriate methodology for drought screening [84]. Simultaneous screening for resistance to multiple biotic and abiotic stresses could be more beneficial to improve yield under multiple stress-prone environments. 4.1.1. Secondary Traits Secondary traits are distinct components of prime plant traits such as grain yield. Secondary traits are important indicators of different physiological, molecular, and developmental changes involved in drought resistance, tolerance, and adaptation mechanisms. The effectiveness of selection for secondary traits such as root thickness, penetration ability and depth, greater hydraulic conductance, xylem thickness and osmotic adjustment, leaf area [85,86], leaf water potential [87], fresh and dry root weight, root volume, relative water content [26], root length [25], photosynthesis [88], early flowering, and harvest index [89] in rice to improve yield under drought is yet to be successfully demonstrated. This also goes for the anthesis-silking interval in maize [90], greenness in sorghum [91], Agronomy 2017, 7, 27 7 of 27 and water-use efficiency in wheat [92]. Improvement in yield potential and yield stability across variable environments has also been reported by considering stay-green [93,94], an essential trait in several crops (maize, rice, sorghum) that gives plants resistance to drought, premature senescence [95], and lodging. Selection for effective mobilization of the reserves from source to sink [96], osmoregulation [97], cuticular resistance, surface roughness [98], and membrane composition [99] suggested the importance of these traits in reducing drought-dependent yield loss. Stomatal conductance, maximal rates of photosynthesis [100], and developmental plasticity [101] were reported to be positively correlated, whereas leaf temperatures were negatively correlated with yield increase under stress in semi-dwarf spring wheat cultivars [100]. Another example of a successful breeding program for drought stress using carbon isotope discrimination as a substitute for water-use efficiency in increasing yield in wheat was reported by Rebetzke et al. [102] and Cattivelli et al. [103]. The limitations associated with these techniques involved the screening of only a limited number of plants because of high cost and screening under controlled conditions that may not reflect field conditions. A number of putative secondary traits such as root density, root thickness, root distribution pattern [104,105], rooting depth [106,107], root branching, root-to-shoot ratio, root penetration [108–112], root length, root hydraulic conductance, transpiration demand [113], and water and nutrient uptake [111,114,115] have been suggested to confer drought tolerance [116]. Traits such as transpiration rate, biomass accumulation, stomatal conductance, leaf area [117–119], osmoregulation [93], relative water content, and leaf water potential [120] reported a positive association with grain yield under drought stress. Various reports suggested the role of genetic regions associated with secondary traits (Table 4, [121–136]) in enhancing grain yield under drought stress. Table 4. Genetic regions reported to be associated with secondary traits enhancing drought tolerance. Crop Rice Chr Root-shoot growth, deep root growth [109,121] 9 Root length, root thickness, straw yield [122,123] 12 Biomass, panicle number, lateral root, panicle branching [124,125] Wheat 2A, 2B, 3A, 3B, 5A, 5B, 6B, 7A, 6HL [126] Osmotic adjustment [126,127] Relative water content, leaf osmotic potential, osmotic adjustment, carbon isotope discrimination [128–130] Carbon isotope discrimination [131] 2H, 4H, 6H, 7H Chlorophyll, fluorescence [132] 2H, 3H, 4H, 5H Cotton Carbon isotope ratio, osmotic potential, chlorophyll content, flag leaf, rolling index 2H, 3H, 6H, 7H 1H, 2H, 3H, 5H, 6H,7H Sorghum Reference 1 2B, 4A, 5A, 7B Barley Trait Improved Relative water content [133,134] Osmotic potential [134] 1, 2, 3, 4 Leaf area, delayed leaf senescence, stay green [91] 06, 02, 25 Biomass production; panicle number, specific, leaf weight and chlorophyll, osmotic potential, stomatal density, stomatal conductance [135,136] Agronomy 2017, 7, 27 8 of 27 4.1.2. Grain Yield as a Selection Criterion under Drought Even though screening for physiological traits is more accurate than the screening of complex quantitative agronomic traits, drought is still a complex process involving multiple steps starting from moisture-nutrient uptake by roots to grain formation by the panicle. Each physiological trait in turn fulfills one or two of the multiple sequential components needed to produce higher yield. Moreover, the appropriate combinations of these components to achieve increased yield under drought are not well understood. Grain yield, being a complex quantitative trait, was not considered earlier as a suitable selection criterion in breeding [93,105,137]. On the contrary, exploitation of genetic variation using direct selection for the trait for grain yield under drought and combining high yield potential with this trait has now been suggested as an appropriate alternative [138–142]. Several studies on comparative phenotypic screening of breeding material for grain yield under reproductive-stage drought stress Agronomy 2017, 7, 27 8 of 26 and under a controlled environment [138–143] showed moderate heritability of grain yield under drought stress. of Several experiments to standardize the procedure screening involving heritability grain yield under drought stress. Several experimentsoftophenotypic standardize the procedure of directphenotypic selection for grain yield as selection criteria (Figure 3) reported grain yield advantage under screening involving direct selection for grain yield as selection criteria (Figure 3) reproductive-stage stress with comparable yield under irrigated situations in uplandsyield [53] and reported grain drought yield advantage under reproductive-stage drought stress with comparable under[50,144], irrigatedand situations in uplands [53] and lowlands [50,144], and in multiple locations This lowlands in multiple locations [145]. This type of cyclical stress will allow[145]. development, type of cyclical stress willfor allow development, phenotyping, and selection for of drought resistance phenotyping, and selection drought resistance in populations consisting genotypes withinbroad populations consisting of genotypes with broad growth duration. growth duration. Figure 3. Standardized protocol for drought phenotyping screening IRRI. DAS: days Figure 3. Standardized protocol for drought phenotyping screening at at IRRI. DAS: days afterafter seeding, seeding, DAT: days after transplanting. DAT: days after transplanting. 4.1.3. High-Throughput Screening 4.1.3. High-Throughput Screening The new tools of phenomics, such as carbon isotope discrimination (CID) [146], infrared The new toolscanopy of phenomics, such as [104,147], carbon isotope discrimination (CID) [146], infrared thermography, spectral reflectance pulse amplitude-modulated fluorometry for thermography, spectral amplitude-modulated fluorometry chlorophyll canopy fluorescence [148],reflectance normalized[104,147], differencepulse vegetation index (NDVI) [149] and for chlorophyll fluorescence [148],(PRI) normalized difference vegetation index(PET), (NDVI) [149] and photosynthetic reflective index [150], positron emission tomography magnetic resonance imaging nuclear [151,152] are now available to better photosynthetic reflective(MRI), indexand (PRI) [150],magnetic positronresonance emission tomography (PET), magnetic resonance understand the contribution of different morpho-physiological traits to grain yield. Planes, airborne imaging (MRI), and nuclear magnetic resonance [151,152] are now available to better understand the instruments, and moving equipment with multispectral sensors canPlanes, estimate the plant cover and and contribution of different morpho-physiological traits to grain yield. airborne instruments, nutrient needs of crops. The information collected from phenomics tools such as a high-density soil moving equipment with multispectral sensors can estimate the plant cover and nutrient needs of crops. map to track porosity and mineral content, detectors to predict nutrient content and changes in The information collected from phenomics tools such as a high-density soil map to track porosity response to inputs, contour mapping to observe water movements, and soil moisture detectors at multiple depths, when combined with GPS data, can give useful information about land productivity and will be useful for the following season’s planting pattern. Well-developed analytical tools/packages are essential for analyzing and interpreting the large amount of data produced by these modern techniques in the future. Agronomy 2017, 7, 27 9 of 27 and mineral content, detectors to predict nutrient content and changes in response to inputs, contour mapping to observe water movements, and soil moisture detectors at multiple depths, when combined with GPS data, can give useful information about land productivity and will be useful for the following season’s planting pattern. Well-developed analytical tools/packages are essential for analyzing and interpreting the large amount of data produced by these modern techniques in the future. 4.2. Breeding Strategies Research work is needed in breeding rice varieties with high grain yield potential, good yield under drought, yield stability, resistance to existing biotic stresses, good grain and cooking quality, and good relative performance in multiple locations and environmental (managed under drought-stress and non-stress environments) conditions. 4.2.1. Donor Identification The preliminary and important step of any breeding program involves the identification of suitable donors. Selection of a specific donor from a large germplasm collection is a crucial step. The use of a specific donor with special characteristics for a specific environment may lead to the success of any varietal and trait development program. Most of the traditional donors have several undesirable traits and therefore are not suitable for direct use in any breeding program. These landraces have undesirable traits such as little ground cover, tall plant height, low yield potential, and poor grain and eating quality, but they have a desirable drought tolerance trait. On the other hand, modern rice varieties have desirable traits such as high yield, improved plant type (early vigor, medium height, and lodging resistance), tolerance of biotic stress, and good grain type (medium to long slender). However, they are drought-susceptible. Breeding for any desired trait to get new gene combinations requires exploitation of genetic variation (intra-specific, inter-specific, or inter-generic) that exist in traditional landraces carrying desirable characteristics and modern improved varieties with high yield potential [153]. The genotype at par performance in the target environment [154] and the trait with high heritability [155] can account for further high-throughput screening. The identified drought-tolerant donors such as PSBRc68, PSBRc80, PSBRc82, Aday Sel, Dagaddeshi, Kali Aus, Aus276, Kalia, N22, Apo, Dular, and IR77298-14-1-2 have been used in conventional breeding and QTL mapping studies at IRRI. Among these, improved donors such as PSBRc68, PSBRc80, PSBRc82, and IR77298-14-1-2 have been directly used in conventional breeding programs, whereas improved drought-tolerant lines free from undesirable linkages were derived from the mapping populations that involve traditional donors such as Aday Sel, Dagaddeshi, Kali Aus, Aus 276, Kalia, N22, Apo, and Dular and used in conventional breeding programs. In marker-assisted breeding programs, lines possessing the identified QTLs for grain yield under drought, which come from mapping populations that involve traditional donors, were used to improve mega-varieties. A model drought-resistant rice variety for drought-prone environments can be considered as having better yields than any other presently available cultivar, not only under drought stress but also under irrigated conditions across different seasons and environments, being less sensitive to variable conditions [83,156–158], and possessing good grain quality and resistance to biotic stresses. 4.2.2. Conventional Breeding Over the last 10 years, conventional breeding at distinguished worldwide research centers has made significant progress in developing biotic and abiotic stress-tolerant lines/cultivars of some important food crops such as chickpea [159], soybean [160], wheat [161–163], barley [164,165], rice [89], and common bean [166] using different protocols and designs. The drought breeding program at IRRI has led to the development of several high-yielding, drought-tolerant lines with a release of varieties across South and Southeast Asia and Africa since 2009 (Table 5). However, it is time-consuming, costly, and labor-intensive, and there is a high probability of transferring undesirable genes. A modified conventional breeding approach (Figure 4) involving an integrative sequential Agronomy 2017, 7, 27 10 of 27 phenotyping, genotyping, and selection strategy to screen a large number of plants will improve the assessment of plant response to drought stress. This efficient, precise, cost-effective breeding approach may expedite the development of drought-tolerant rice varieties with a high frequency of favorable genes. Table 5. High-yielding drought-tolerant varieties released from IRRI’s drought breeding program. Name Designation Country Katihan 1 IR 79913-B-176-B-4 Philippines Sahod Ulan 3 IR 81412-B-B-82-1 Philippines Sahod Ulan 5 IR 81023-B-116-1-2 Philippines Sahod Ulan 6 IR 72667-16-1-B-B-3 Philippines Sahod Ulan 8 IR 74963-262-5-1-3-3 Philippines Inpago LIPI Go 1 IR 79971-B-191-B-B Indonesia Agronomy 2017, 7, 27 Inpago LIPI Go 2 IR 79971-B-227-B-B Indonesia CR dhan 40 IR 55423-01 India Sahod Ulan 5 IR 81023-B-116-1-2 Philippines Sahod Ulan 12Sahod UlanIR 81047-B-106-2-4 Philippines 6 IR 72667-16-1-B-B-3 Philippines Mozambique M’ZIVA Sahod Ulan 8R77080-B-B-34-3 IR 74963-262-5-1-3-3 Philippines CR dhan 201Inpago LIPI Go IR183380-B-B-124-1 India IR 79971-B-191-B-B Indonesia 2 84899-B-154 IR 79971-B-227-B-B Indonesia CR dhan 202Inpago LIPI Go IR India IR 55423-01 India CR dhan 204 CR dhan 40IR 83927-B-B-279 India 12 IR 81047-B-106-2-4 Philippines Sukha dhan 5Sahod UlanIR 83388-B-B-108-3 Nepal M’ZIVA R77080-B-B-34-3 Mozambique Sukha dhan 6 CR dhan 201 IR 83383-B-B-129-4 Nepal IR 83380-B-B-124-1 India BRRI dhan 66 CR dhan 202IR 82635-B-B-75-2 Bangladesh IR 84899-B-154 India Katihan 3 CR dhan 204 IR 86857-101-2-1-3 Philippines IR 83927-B-B-279 India IR 83388-B-B-108-3 Nepal DRR dhan 43 Sukha dhan 5 IR 83876-B-RP India 6 93376-B-B-130 IR 83383-B-B-129-4 Nepal DRR dhan 44 Sukha dhan IR India BRRI dhan 66 IR 82635-B-B-75-2 Bangladesh Katihan 2 IR 82635-B-B-47-2 Philippines Katihan 3 IR 86857-101-2-1-3 Philippines BRRI dhan 71 DRR dhan 43 IR 82589-B-B-84-3 Bangladesh IR 83876-B-RP India Swarna ShreyaDRR dhan IR 84899-B-179-16-1-1-1-1 India 44 IR 93376-B-B-130 India Sahod Ulan 15 Katihan 2IR 83383-B-B-129-4 Philippines IR 82635-B-B-47-2 Philippines IR 82589-B-B-84-3 Bangladesh Sahod Ulan 20BRRI dhan 71IR 86781-3-3-1-1 Philippines IR 84899-B-179-16-1-1-1-1 Malawai India MPTSA Swarna Shreya IR 82077-B-B-71-1 IR 83383-B-B-129-4 Philippines ATETE Sahod Ulan 15IR 80411-B-49-1 Malawai Sahod Ulan 20 IR 86781-3-3-1-1 Philippines CAR 14 IR80463-B-39-3 Cambodia MPTSA IR 82077-B-B-71-1 Malawai Identified Philippines ATETE IR 84878-B-60-4-1 IR 80411-B-49-1 Malawai a Ecosystem a UP RL RL RL RL UP UP UP RL RL RL RL RL Aerobic UP UP Aerobic UP Aerobic RL RL RL RL Aerobic RL Aerobic UP Aerobic RL RL RL RL RL UP UP RL RL RL RL RL UP RL RL RL RL IR,RL RL RL IR,RL RL RLRL IR, 2011 2011 2011 2011 2011 2011 2011 2012 2011 2013 2011 2011 2013 2011 2014 2011 2014 2012 2014 2013 2014 2013 2014 2014 2014 2014 2014 2014 2014 2014 2014 2014 2014 2014 2014 2015 2014 2014 2015 2014 2015 2015 2015 2015 2015 2015 2015 2015 2015 2015 2015 2016 CAR 14 IR80463-B-39-3 Cambodia RL 2015 UP: upland, RL: rainfed lowland, IR—irrigated ecology.IR,RL Source: Modified Identified IR 84878-B-60-4-1 Philippines 2016 a Days to Maturity Release Year 115 115 125 110 113 110 105 120 118 115 110 125 125 113 107 115 115 107 115 112 115 115 120 118 115 from 113 Plant Height (cm) 105 120 115 115 125 110 11310 of 26 110 130 105 100 120 100 118 115 114 115 100 110 119 125 130 125 100 113 100 107 100 105 115 105 115 116 107 87 115 105 112 105 115 84 112 115 121 120 110 118 112 115 110 113 112 90 107 130 100 100 115 114 100 119 130 100 100 100 105 105 116 87 105 105 84 112 121 110 112 110 112 110 97 110 Kumar et al. [89]. 97 UP: upland, RL: rainfed lowland, IR—irrigated ecology. Source: Modified from Kumar et al. [89]. Figure 4. Modified conventional breeding approach. OYT: Observational yield trials, AYT: advanced Figure 4. Modified conventional breeding approach. OYT: Observational yield trials, AYT: advanced yield trials, MET: multi environmental trials. yield trials, MET: multi environmental trials. 4.2.3. Marker-Assisted Breeding: Identification, Introgression, and Pyramiding of QTLs Marker-assisted breeding adopted at IRRI involves: the development of mapping populations involving traditional drought-tolerant donors and modern high-yielding varieties; precise phenotyping in multi-environment, controlled, and drought-stress conditions; repeated years;