Preferential Geographic Distribution Pattern of Abiotic Stress Tolerant Rice
© The Author(s). 2018
Received: 11 September 2017
Accepted: 17 January 2018
Published: 8 February 2018
Crop productivity and stability of the food system are threatened by climate change, mainly through the effects of predicted abiotic stresses. Despite extensive research on abiotic stress tolerance in the past decades, the successful translation of these research to fields/farmers is scarce. The impelling demand of climate resilient varieties, and the poor translation of research into the field despite the availability of high throughput technologies lead us to critically analyse a neglected aspect of current abiotic stress tolerance research. Although environmental factors play the most important role in the development of adaptive traits of plants, most abiotic stress tolerance research ignores eco-geographic aspects of highly stress tolerant accessions. In this review, we critically examined the geographic distribution pattern of highly tolerant rice accessions of all major abiotic stresses along with one micronutrient deficiency. Remarkably, we identified a shared geographic distribution pattern of highly tolerant accessions for all abiotic stresses including zinc deficiency despite the sparseness of highly tolerant accessions. The majority of these tolerant accessions predominately originated from Bangladesh centred narrow geographic region. We therefore analysed the climatic and agro-ecological features of Bangladesh. Considering the threat of climate change on global food security and poverty, urgent concerted research efforts are necessary for the development of climate resilient rice varieties utilizing the technological advancement, know-hows, and the preferential distribution pattern of abiotic stress tolerant rice.
Poverty, food insecurity, and climate change are the three prime global challenges. Considering their impacts, all three were chosen for the 2030 agenda for sustainable development goals by the United Nations (UN General Assembly, 2015). However, among these three, the interrelation between climate change and food security, and more specifically agricultural production are well documented (Schmidhuber and Tubiello 2007; Lobell et al. 2008; Wheeler and von Braun 2013; Brown et al. 2015). All climate-modelling studies predict that climate change is likely to change precipitation patterns (resulting in more drought or floods), rise of temperature (heat stress) and sea levels (flood and saline intrusion), occurrence of more frequent and severe weather extremes (drought/flood/cyclone etc.). Weather extremes significantly reduce crop production, and can even destroy complete crop production in severe cases. It has been estimated that unfavourable climatic conditions and inappropriate soil can account for over 70% of the yield loss of major crops (Boyer 1982).
Rice is the single most important primary food source crop for half of the world’s population (GRiSP 2013). Nearly all rice is produced (90%) and consumed (87%) in Asia. Overall, rice accounts for nearly 30% of the calorie demands for more than 3 billion Asians. However, in many rice-consuming countries like Bangladesh, Cambodia, Indonesia, and Vietnam, rice makes up for 45-70% of the calorie requirements (GRiSP 2013). Nevertheless, the majority of the population in rice-producing areas, particularly in numerous Asian and African countries, still suffer from hunger, malnutrition and extreme poverty. It was projected that global rice production need to be doubled by 2030 to cope with the impending population demand. However, although rice production has increased over three-fold in the last 4 decades, the growth rate of rice yield is far below the required projected demand (Ray et al. 2013). Moreover, the impact of climate change on agriculture (IMPACT modelling) predicts that global rice production will decline by 12-14% by 2050 compared to the 2000 production baseline (Nelson et al. 2009). Therefore, it will be impossible to meet the demand of increasing global population of almost 10 billion by 2050, unless revolutionary innovations similar to the green revolution of the 1960s or hybrid rice of the 1970s are forthcoming. These include technological interventions, reduction of production loss, expansion of rice cultivation in sub-optimal conditions (problem and saline soils) and the development of climate resilient varieties.
Gene mining and subsequent genetic manipulation are key technologies in abiotic stress tolerance research (Cabello et al. 2014; Mickelbart et al. 2015). However, although this reductionist approach has successfully characterized the function of a significant number of genes, the translation of these research outcomes into the field is scarce (Nelissen et al. 2014; Groen and Purugganan 2016; Gilliham et al. 2017) and the release of improved varieties is even rarer. The release and adoption of flash flood tolerant SUB1 rice varieties in several Asian countries are a notable example of the successful translation of research to fields/farmers although these varieties were developed through a marker-assisted backcrossing (MABC) strategy (Ismail et al. 2013). SUB1A, the master regulator of flash flood tolerance was identified from FR13A, a pure line selection from the local landrace, Dhalputtia grown in the Indian state of Orissa. The breakthrough point was the identification of a single QTL on chromosome 9 explaining nearly 70% of the phenotypic variation (Xu and Mackill 1996). Later, a specific gene was identified after concerted research efforts (Xu et al. 2006). Subsequently, multiple varieties were developed and released in several countries after field trials in numerous countries (Septiningsih et al. 2013). The success of SUB1 rice may be plausibly due to single gene regulated stress tolerance. Such a success story is unlikely to be repeated in other abiotic stress tolerances as dozens/hundreds of QTLs/genes have already been reported for their role in the respective stress tolerances (Cabello et al. 2014; Hu and Xiong 2014; Roy et al. 2014; Todaka et al. 2015; Ohama et al. 2017; Shakiba et al. 2017) and none of them can singly explain such high-level variations.
The stagnation of successful translation of abiotic stress tolerance research to fields/farmers is a growing concern (Nelissen et al. 2014; Groen and Purugganan 2016; Gilliham et al. 2017). This is emphasized by the impelling demand of climate resilient varieties because of the predicted impact of climate change on crop productivity together with the impending population demand. However, although current reductionist research has successfully identified and characterized significant numbers of abiotic stress tolerant genes (mostly in controlled environments), numerous factors of crop fields including macro/micro climate, seasonality, etc. are more highly diverse than can be simulated in controlled growth chambers or greenhouses. Therefore, increased stress tolerance of a transgenic plant in controlled growth chamber or greenhouse does not warrant the same performance in field conditions. In addition, almost all stress tolerance studies have simply overlooked the environmental aspect of stress tolerance, more specifically the eco-geographic aspect of stress-tolerant germplasms. However, environmental factors play an equally important role in the development of adaptive traits of plants. Simply put, whatever the genetic basis of the tolerance of a particular stress-tolerant local landrace, the tolerance was developed/acquired through recurrent exposure to the particular stress in a specific geo-climatic area and directional selection, either by farmers in domesticated crops or by nature. Put it in other words with a specific example; Why is Dhalputtia, the ultimate landrace from which SUB1A was identified, in Orissa, India; but not in Gansu, China or Sapporo, Japan? How important is the geolocation of tolerant accession? Is there any pattern of geolocation among abiotic stress tolerant rice accessions? An extraordinary genome-environment association study using the model plant Arabidopsis thaliana (Fournier-Level et al. 2011) clearly showed local adaption, and more specifically high fitness alleles were generally distributed closer to the site of specific and distinct climatic spaces. However, this kind of study has yet to be applied to rice accessions.
Generalized Standard Evaluation System for rice (SES)
General Descriptionb and Desirability
Cold Stress at Seedling Stagec
Absence of visible symptoms or injury
no damage to leaves, normal leaf color
Potential donor of the trait
Trait expression is satisfactory
tip of leaves slightly dried, folded, and light green
Potential donor of the trait
Trait expression is not as good as it should be, but may be acceptable under some circumstances
leaves of seedlings are severely rolled and dried
Trait expression is unsatisfactory (not useful)
the majority of the seedlings died and dried
Generally, abiotic stresses are studied, analysed, and even reviewed separately; rarely multiple stresses are analysed together. However, in this review, we have critically analysed the geographic distribution patterns of highly stress tolerant rice accessions for all major abiotic stresses along with one micronutrient deficiency. If the geographic distribution pattern of abiotic stress tolerant accessions showed a shared pattern, then the genetic basis of local adaptation or high fitness alleles can be identified through further studies utilizing the advances in genome research tools and know-hows such as genome sequencing and genome wide association studies (GWAS). Remarkably, the cost of genome sequencing has been drastically reduced in the last two decades due to the revolutionary advancement of DNA sequencing technologies. Therefore, sequencing of thousand accessions is no longer a dream project and has already become a reality (Alexandrov et al. 2014). Thus, we have now both the toolbox as well as the know-how to identify the genetic signature from big-data, we just need an effective approach to overcome the limitations.
Therefore, in this review, we have explicitly examined the results of large-scale screening of abiotic stress tolerance to identify the preferential geographic distribution patterns of all major abiotic stress-tolerant rice accessions. Abiotic stresses include cold, salt, alkali, drought, and both flash and prolonged floods. Alkaline (sodic) soils are usually zinc deficient, therefore, we have also analysed zinc deficiency tolerant accessions to confirm whether salt, alkali and zinc deficiency tolerant accessions show a shared pattern.
Geographic Distribution Pattern of Abiotic Stress Tolerant Rice Accessions
To reconfirm the area of preference of salt tolerant rice accessions, we analysed the results of a recent medium-scale screening (Platten et al. 2013) that comprised hundreds of accessions of both of the cultivated rice, Oryza sativa and O. glaberrima. However, although only seven accessions of O. sativa were found highly tolerant in that study, highly tolerant accessions were also prevalent in Bangladesh (Bangladesh 4, India 1, Philippines 1, and Thailand 1). We analysed the geographic distribution pattern of the 50 salt tolerant accessions (7 and 43 accessions of highly tolerant and tolerant category, respectively). Interestingly, the preferred latitude, longitude, and the area of preference of salt tolerant accessions remained the same (Additional file 1: Figure S1a-c, identical to the large-scale screening, Fig. 1b-g). Thus, the recurrence of Bangladesh as the area of preference of highly salt tolerant rice accessions in independent studies clearly validated the specific distribution pattern of salt tolerant rice.
Zinc Deficiency Tolerance
Prolonged Flood Tolerance
Flash Flood Tolerance
Anaerobic Germination (AG) Tolerance
Between 1978 and 1985, nearly 40,000 germplasms (accessions and breeding lines) were screened for the best drought tolerant germplasm; however, the majority of the top 20 outstanding germplasms were breeding lines (de Datta et al. 1988). The sources of tolerance in breeding lines are often obscure as the breeding process involves numerous parents. For instance, the ancestry of the most popular rice variety, IR64 includes 19 landraces from nine different countries (Khush and Virk 2005). All these large-scale drought and related screening results clearly showed that drought tolerance largely depends on growth stage, severity of drought and the specific environmental conditions. Most importantly, drought tolerance for vegetative stages does not correlate with yield performance under water stress. Moreover, drought stress breeding is challenging due to the lack of suitable screening methods.
A recent selection approach, i.e., direct selection for yield performance in both drought and well-watered conditions seems a most effective selection strategy and has been increasingly accepted for drought tolerance studies in rice (Kumar et al. 2008; Venuprasad et al. 2008; Torres et al. 2013). Using this strategy, 988 accessions originated from 47 countries were screened in fields for yield performance under drought and well-watered conditions during 2004-2009 (Torres et al. 2013). We analyzed the geographic distribution pattern of the tolerant accessions (Fig. 8 j-k) identified in that study. Remarkably, both latitude- and longitude-wise distribution patterns of the drought tolerant accessions also clearly showed a single peak preference where the preferred latitude (20-24°N) and longitude (80-100°E) were identical to other abiotic stress tolerances (Fig. 8j-i). The preferred area of drought tolerance within the preferred latitude and longitude comprised more than half of the tolerant accessions (74% considering the entire countries). India accounted for marginally more tolerant accessions than Bangladesh (Fig. 8l); however, the majority of the Indian accessions originated from Bangladesh adjacent states. Moreover, recommended varieties for drought stress breeding such as Kataktara Da2, Dular, Shada Shaita, and DA 28 (Torres et al. 2013) also originated from Bangladesh and most of them are still being cultivated in considerable areas in Bangladesh (Hossain et al. 2013). Therefore, based on the consistent prevalence of drought tolerant accessions in Bangladesh centred area in both reproductive stage drought screening as well as direct selection by yield performance, we considered Bangladesh centred area also the area of preference of drought tolerant rice accessions.
To compare and experimentally verify the cold tolerance capacity of Rayada rice, we imposed a cold stress of 10 °C for a continuous 21 days on 35 day old seedlings in a growth chamber. Interestingly, all of the indica rice varieties we screened, including high yielding cold tolerant indica variety, BRRI 36 completely died and were dessicated in the prolong cold exposure (Fig. 10c-e). In contrast, Rayada rice accessions showed a similar cold tolerance ability to the two temperate japonica varieties, Nipponbare and Dongjin. Remarkably, the recovery performance of Rayada varieties was even better than that of the japonica varieties (Fig. 10e). To reconfirm the cold tolerance of mature Rayada plants under field conditions, we grew different rice varieties including Rayada rice in the CUHK gene garden in three consecutive winter seasons from 2014 to 2016. However, winter temperature of 2014, 2015 did not drop below 10 °C on consecutive days. Fortunately, between 22 and 27 January of 2016, the temperature of Hong Kong dropped below 10 °C for 5 consecutive days (Fig. 10 f). Remarkably, the temperature of 24th January 2016 was 3.1 °C which is the lowest recorded temperature for over 50 years in Hong Kong. Exposure to these chilling temperatures on Rayada varieties showed no symptoms (Fig. 10 g) while leaves of indica varieties became severely rolled and dried (Fig. 10 h). Thus, cold tolerance ability of Rayada rice in both seedling and mature plants were experimentally confirmed.
Agro-climatic Features of the Area of Preference for All Abiotic Stress Tolerance Rice
Based on physiography, soil types, hydrology and agro-climatic features, Bangladesh is divided into 30 agro-ecological zones. However, due to year-round suitable agro-climatic conditions, rice is cultivated throughout the year with overlapping or short turnover periods; mainly in three seasons: aus (Mar-July), aman (May-Dec) and boro (Dec-June). Aman rice are of two types- broadcast aman and transplanted aman. Broadcast aman is a direct seeded traditional deepwater rice which matures after the monsoon period, i.e., mostly during Nov-Dec whereas transplanted aman is rainfed, sometimes irrigated. Aus and broadcast aman are cultivated in the upland and deepwater ecosystems, respectively. Boro rice is usually transplanted in Dec-Jan and is harvested before monsoon. Aman is the main rice cropping season since time immemorial in Bangladesh; the oldest Bengali literature, Charyapada only mentions aman rice. However, cultivation areas of broadcast aman and aus have been significantly decreased (over 80% and 60%, respectively) in the last four decades (Additional file 2: Figure S2). Broadcast aman (prolong flood tolerant rice) and aus (drought tolerant) are known for their stress tolerance capacity since they are grown during stress prone seasons. Boro cultivation area was sharply increased (over five-fold) in the last 5 decades (Additional file 2: Figure S2), mostly because of the expansion of irrigation facilities and the higher yield of modern varieties.
Flooding is the most prevalent and recurrent abiotic stress in Bangladesh due to its agro-ecological and geo-climatic features. The majority of the cultivable areas of Bangladesh are in floodplains and therefore flood-prone (Fig. 12a) with distinct types, intensities and depth (Fig. 12a, b). Millions of hectares of cultivable areas are in risk of either river flooding or flash floods. In addition, over 2 million hectares are in danger of tidal surges (Fig. 12a). Over 10% of the areas of the total flood-prone zones may experience a flooding depth over 1.8 m. The majority of the area of rabi and pre-kharif seasons are also drought-prone due to the combined effect of climatic (Fig. 11) and agro-ecological features of the pre-monsoon season (March to May). However, the severity of drought depends on the land types of particular region, their soil texture and moisture holding capacity, permeability, drainage and number of dry days etc. Apart from drought and flood, a few other constraints: salinity, alkaline and acid sulphate soils hamper rice cultivation and expansion in Bangladesh (Fig. 12d and Additional file 3: Figure S3). However, although the majority of the cultivable land are non-saline, hundreds of thousands of hectares of land, particularly in the costal belt areas (Additional file 3: Figure S3), suffer from salinity to various extents.
Sparseness of Highly Abiotic Stress Tolerant Rice Accessions
Preferential Geographic Distribution Pattern of Abiotic Stress Tolerant Rice Accessions
Total number of accessions screened
Highly tolerant accessionsa
Highly tolerant accessions (%)
No of highly tolerant accessions from Bangladesh
Highly tolerant accessions from Bangladesh (%)
Flooded seed germination (AG)
Drought - yield performance
Drought -non-yield performance screening
Earlier we analysed preferential distribution pattern and population types of drought and flood tolerant rice accessions (Bin Rahman and Zhang 2016). However, in this review, we analysed all seven major abiotic stresses along with one nutrient deficiency tolerance. Surprisingly, Bangladesh has turned out to be the area of preference for highly tolerant accessions of all of the abiotic stresses along with one nutrient deficiency. In some cases, almost all of the highly tolerant accessions originated from Bangladesh or Bangladesh centred area (Table 2 and additional file 4: Table S1). Natural coincidence of the areas of preference of the 7 abiotic stresses along with one nutrient deficiency in a narrow geographic region is literally impossible; rather it is the specific pattern of preferential distribution of abiotic stress tolerant rice accessions. More surprisingly, Bangladesh is one of the most vulnerable climate change countries of the world where rice is literally the nutritional lifeline. On the average, rice accounts for nearly 70% of the calorific demand in Bangladesh (GRiSP 2013), where poor people basically live solely on rice. Bangladesh is the only rice-growing country where rice is represented in both the country’s national anthem and national emblem. Bangladesh is a relatively very small country (area only 147,570 km2); 65, 22 and 12 times smaller than the other top three rice producing countries, China, India, and Indonesia, respectively. However, Bangladesh is the 4th largest rice producer of the world (GRiSP 2013), where still hundreds of traditional rice varieties are cultivated (Hossain et al. 2013).
Aus rice varieties are well known for their abiotic stress tolerance capacity. Cultivation of aus rice is confined to Bangladesh and adjacent Indian states. The most primitive deepwater rice ecotype, Rayada, is often categorized as aus although some studies identified it as a distinct population type (Glaszmann 1987). No Bangladeshi accessions was screened in greenhouse screening for zinc deficiency tolerance, hence we see a gap in the longitude wise distribution (Fig. 3g arrow). However, if we fill the gap using the zinc deficiency field screening data pattern, then clearly it shows the same single peak preference and, as expected, it lies in Bangladesh. AG tolerant accessions are amongst the rarest of all abiotic stresses. However, from 6, 2 Bangladeshi rice accessions (Khaiyan, Kalongchi) are still highly tolerant. More interestingly, only two countries (India and Myanmar) share a border with Bangladesh where both of the countries also possess one AG tolerant rice accession each (India -Nanhi; Myanmar-Khao Hlan On). The largest QTL effect identified for AG tolerance, qAG-9-2 (also known as AG1), was identified from Myanmar landrace, Khao Hlan On (Angaji et al. 2010). Kretzschmar et al. (2015) identified a trehalose-6-phosphate phosphatase gene, OsTPP7, as the genetic determinant in qAG-9-2. Recently, the QTL was successfully introgressed into the elite cultivars/mega varieties like IR64, Ciherang to produce Sub1 + AG1 rice lines via MABC. Nearly 75% of drought tolerant accessions also originated from Bangladesh and adjacent Indian states. Likewise, PSTOL1 (Gamuyao et al. 2012) and SUB1A (Xu et al. 2006) were also identified from the landraces of the same region. Therefore, the preferential geographic distribution of abiotic stress tolerant rice accessions in Bangladesh or Bangladesh centred areas is undoubtedly the shared distribution pattern.
Implication of the Specific Distribution Patterns of Abiotic Stress Tolerant Rice
We need to capitalize on the patterns for the development of abiotic stress tolerant rice varieties as well as the genetic and evolutionary bases of the preferential distribution pattern. Origin and domestication history of rice could help us to understand the specific distribution pattern of abiotic stress tolerant accessions. However, both origin and the place of rice domestication have long being highly debated topics. Vavilov (1926) considered India (Bangladesh was then part of India, became independent in 1971) as the place of rice domestication. A similar conclusion was drawn in later reports (Ramiah and Ghose 1951; Sampath and Govindaswamy 1958) based on the ecological similarities between wild and cultivated rice. However, some Chinese scientists have differed, and considered instead China to be the place of domestication as De Candolle postulated earlier (Oka 1988). Numerous small to large-scale studies have been carried out in the last couple of decades to put an end to these debates. Recently, based on the sequencing of thousands of accessions of wild and cultivated rice it was concluded that the Guangxi province of China as the most likely place of the first development of cultivated rice (Huang et al. 2012). However, the debate did not stop there as a re-analysis of the same dataset by a different group (Civáň et al. 2015) concluded multiple domestication centers of rice. Against this, the original authors argued that the reanalysis methods may be technically flawed (Huang and Han 2015). However, the preferential geographic distribution pattern of all major abiotic stress tolerant rice in Bangladesh or Bangladesh centred areas clearly suggest otherwise.
Recently, several agronomically important genes such as SUB1A (Xu et al. 2006), SNORKEL (Hattori et al. 2009), PSTOL1 (Gamuyao et al. 2012), DRO1 (Uga et al. 2013) have been identified from, FR13A, Gowai 38-9, Kasalath, Kinandang Patong, respectively. Except for Kinandang Patong, all other accessions also originated from the identified preferred Bangladesh centred areas/region. An earlier report considered Kinandang Patong as being a tropical japonica variety (Uga et al. 2008). However, recent sequencing-based population and genetic studies (Huang et al. 2012) confirmed it as a typical aus. Cultivation of aus rice is mostly confined to the identified preferred region. However, although the origin and evolution of cultivated rice are beyond the scope of this review, the preferential geographic distribution pattern of the highly tolerant accessions of all seven major abiotic stresses including cold along with one nutrient deficiency tolerance in a narrow geographic region of Bangladesh centred area clearly point to Bangladesh centred area as being the center of origin of O. sativa. We should perhaps ignore this interesting academic debate, and pay more attention to the shared distribution patterns of abiotic stress tolerant rice accessions as they can be utilized for the development of climate resilient varieties, as we cannot afford to fail the major global challenges like food security by 2050. The consequences could be catastrophic, costing millions of lives.
We know where exactly the abiotic stress tolerant accessions are clustered. We now have sufficient tools and techniques, e.g. genome sequencing, GWAS, automatic phenotypic platforms, even some sensor-based platforms that can measure field level data, to dig more deeply. More importantly, the genome sequencing costs have significantly decreased over the past decades. Unfortunately, only a few tolerant accessions of these abiotic stresses originating from Bangladesh have been sequenced. Therefore, the next immediate step should be genome sequencing of more highly tolerant rice accessions from Bangladesh to identify the signature of stress tolerance patterns by genome wide association studies. The success of GWAS in the pattern recognition of stress tolerance has already been established in numerous crop plants including rice (Huang et al. 2011).
We propose a concerted research effort to identify the genomic speciality of abiotic stress tolerant rice accessions and subsequent development of climate resilient rice varieties. First, the collection of the indigenous knowledge of stress tolerant rice accessions (locality and their special features known to farmers) in Bangladesh before they disappear. For instance, native farmers of Sylhet, Bangladesh call Kasalath (a well-known aus variety from which the PSTOL1 gene has been identified) as Kasa Lota (young green shoot). Kasa Lota is well known among the greater Sylhet rice farmers for its tolerance in the nutrient poor soil. Second, evaluation (both field and laboratory screening) of more landraces from Bangladesh for abiotic stress tolerances. Third, de novo assembly and deep sequencing of one or more traditional land races, particularly aus as we often experienced the absence of agronomically important genes in the rice reference genome, Nipponbare. For instance, Nipponbare completely lacks SNORKEL, PSTOL1 etc. alleles and possesses only intolerant alleles like SUB1A, DRO1. Therefore, it would not be unlikely to anticipate the absence of master regulator(s) of other stress tolerances in Nipponbare. Fourth, identification of genomic signatures of abiotic stress adaptations by both conventional and modern GWAS studies. However, we need more sophisticated bioinformatics and computational algorithms along with a cloud computing platform as the existing tools and methods are unable to handle the extraordinarily growing scale of data. Fifth, development of abiotic stress tolerant or climate-smart rice varieties through intense breeding efforts capitalizing the MABC strategy even before the identification of the detailed molecular mechanisms of tolerance. For instance, the identification of the genetic basis of the semi-dwarf trait (defective gibberellin 20-oxidase) (Spielmeyer et al. 2002) of the green revolutionary rice, IR8 occurred almost 40 years after the revolution of IR8 made, whereas Sub1A rice was literally developed (Neeraja et al. 2007) before the gene identification (Xu et al. 2006) as MABC required several years.
Considering the impact of climate change on global food security and poverty, urgent concerted research efforts are necessary for the development of climate resilient varieties to cope with the impending population demand by utilizing the technological advancement, know-hows, and the preferential distribution pattern of abiotic stress tolerant rice.
We acknowledge grant supports from Hong Kong Research Grant Council (14122415, 14160516, 14177617, AoE/M-05/12, AoE/M-403/16). We dedicate this article to the memory of Prof. Sheikh Shamimul Alam who guided ANMRBR in masters and early career development.
ANMRBR and JZ conceived the project. ANMRBR did all the experiments and analysis, overall research was supervised by JZ. The manuscript was written by ANMRBR and JZ. Both authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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- Alexandrov N, Tai S, Wang W et al (2014) SNP-seek database of SNPs derived from 3000 rice genomes. Nucleic Acids Res 43:D1023–D1027. https://doi.org/10.1093/nar/gku1039 View ArticlePubMedPubMed CentralGoogle Scholar
- Alloway BJ (2008) Zinc in soils and crop nutrition, 2nd edn. International Zinc Association and International Fertilizer Industry Association, Brussels and ParisGoogle Scholar
- Angaji SA, Septiningsih EM, Mackill DJ, Ismail AM (2010) QTLs associated with tolerance of flooding during germination in rice (Oryza Sativa L.) Euphytica 172:159–168. https://doi.org/10.1007/s10681-009-0014-5 View ArticleGoogle Scholar
- Bin Rahman ANMR, Zhang J (2013) Rayada specialty: the forgotten resource of elite features of rice. Rice 6:41. https://doi.org/10.1186/1939-8433-6-41 View ArticlePubMedPubMed CentralGoogle Scholar
- Bin Rahman ANMR, Zhang J (2016) Flood and drought tolerance in rice: opposite but may coexist. Food Energy Secur 5:76–88. https://doi.org/10.1002/fes3.79 View ArticleGoogle Scholar
- Boyer JS (1982) Plant productivity and environment. Science 218:443–448. https://doi.org/10.1126/science.218.4571.443 View ArticlePubMedGoogle Scholar
- Brown ME, Antle JM, Backlund P et al (2015) Climate change, global food security and the US food system. U.S. Global Change Research Program, Washington, D.C.Google Scholar
- Cabello JV, Lodeyro AF, Zurbriggen MD (2014) Novel perspectives for the engineering of abiotic stress tolerance in plants. Curr Opin Biotechnol 26:62–70. https://doi.org/10.1016/j.copbio.2013.09.011 View ArticlePubMedGoogle Scholar
- Civáň P, Craig H, Cox CJ, Brown TA (2015) Three geographically separate domestications of Asian rice. Nat Plants 1:15164. https://doi.org/10.1038/nplants.2015.164 View ArticlePubMedPubMed CentralGoogle Scholar
- de Datta SK, Malabuyoc JA, Aragon EL (1988) A field screening technique for evaluating rice germplasm for drought tolerance during the vegetative stage. F Crop Res 19:123–134. https://doi.org/10.1016/0378-4290(88)90050-0 View ArticleGoogle Scholar
- Forno DA, Yoshida S, Asher CJ (1975) Zinc deficiency in rice 1. Soil factors associated with the deficiency. Plant Soil 42:537–550. https://doi.org/10.1007/BF00009941 View ArticleGoogle Scholar
- Fournier-Level A, Korte A, Cooper MD et al (2011) A map of local adaptation in Arabidopsis Thaliana. Science 334:86–89. https://doi.org/10.1126/science.1209271 View ArticlePubMedGoogle Scholar
- Gamuyao R, Chin JH, Pariasca-Tanaka J et al (2012) The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488:535–539. https://doi.org/10.1038/nature11346 View ArticlePubMedGoogle Scholar
- Gilliham M, Able JA, Roy SJ (2017) Translating knowledge about abiotic stress tolerance to breeding programmes. Plant J 90:898–917. https://doi.org/10.1111/tpj.13456 View ArticlePubMedGoogle Scholar
- Glaszmann JC (1987) Isozymes and classification of Asian rice varieties. Theor Appl Genet 74:21–30. https://doi.org/10.1007/BF00290078 View ArticlePubMedGoogle Scholar
- GRiSP (2013) Rice almanac, 4th edn. International Rice Research Institute, Los BañosGoogle Scholar
- Groen SC, Purugganan MD (2016) Systems genetics of plant adaptation to environmental. Am J Bot 103:2019–2021. https://doi.org/10.3732/ajb.1600340 View ArticlePubMedGoogle Scholar
- Hattori Y, Nagai K, Furukawa S et al (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460:1026–1030. https://doi.org/10.1038/nature08258 View ArticlePubMedGoogle Scholar
- Hossain M, Jaim W, Alam MS, Rahman AM (2013) Rice Biodiversity in Bangladesh : Adoption, Diffusion and Disappearance of Varieties A Statistical Report from Farm Survey in 2005. Research and Evaluation Division BRAC, DhakaGoogle Scholar
- Hu H, Xiong L (2014) Genetic engineering and breeding of drought-resistant crops. Annu Rev Plant Biol 65:715–741. https://doi.org/10.1146/annurev-arplant-050213-040000 View ArticlePubMedGoogle Scholar
- Huang X, Han B (2015) Rice domestication occurred through single origin and multiple introgressions. Nat Plants 2:15207. https://doi.org/10.1038/nplants.2015.207 View ArticlePubMedGoogle Scholar
- Huang X, Kurata N, Wei X et al (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497–501. https://doi.org/10.1038/nature11532 View ArticlePubMedGoogle Scholar
- Huang X, Zhao Y, Wei X et al (2011) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32–39. https://doi.org/10.1038/ng.1018 View ArticlePubMedGoogle Scholar
- Huke RE, Huke EH (1997) Rice area by type of culture: South, Southeast, and East Asia a revised and updated database. International Rice Research Institute, Los BanosGoogle Scholar
- Iftekharuddaula KM, Ghosal S, Gonzaga ZJ et al (2016) Allelic diversity of newly characterized submergence-tolerant rice (Oryza Sativa L.) germplasm from Bangladesh. Genet Resour Crop Evol 63:859–867. https://doi.org/10.1007/s10722-015-0289-4 View ArticleGoogle Scholar
- IRGCIS (2017) The international Rice Genebank collection information system. http://www.irgcis.irri.org:81/grc/SearchData.html. Accessed 13 June 2017.
- IRRI (2013) Standard evaluation system for rice, 5th edn. International Rice Research Institute, Los BañosGoogle Scholar
- Ismail AM, Ella ES, Vergara GV, Mackill DJ (2009) Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza Sativa). Ann Bot 103:197–209. https://doi.org/10.1093/aob/mcn211 View ArticlePubMedGoogle Scholar
- Ismail AM, Singh US, Singh S et al (2013) The contribution of submergence-tolerant (Sub1) rice varieties to food security in flood-prone rainfed lowland areas in Asia. F Crop Res 152:83–93. https://doi.org/10.1016/j.fcr.2013.01.007 View ArticleGoogle Scholar
- Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34View ArticlePubMedGoogle Scholar
- Khush GS, Virk PS (2005) IR varieties and their impact. International Rice Research Institute, Los BañosGoogle Scholar
- Kretzschmar T, Pelayo MAF, Trijatmiko KR et al (2015) A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice. Nat Plants 1:15124. https://doi.org/10.1038/nplants.2015.124 View ArticlePubMedGoogle Scholar
- Kumar A, Bernier J, Verulkar S et al (2008) Breeding for drought tolerance: direct selection for yield, response to selection and use of drought-tolerant donors in upland and lowland-adapted populations. F Crop Res 107:221–231. https://doi.org/10.1016/j.fcr.2008.02.007 View ArticleGoogle Scholar
- Lobell DB, Burke MB, Tebaldi C et al (2008) Prioritizing climate change adaptation needs for food security in 2030. Science 319:607–610. https://doi.org/10.1126/science.1152339 View ArticlePubMedGoogle Scholar
- Mickelbart MV, Hasegawa PM, Bailey-Serres J (2015) Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nat Rev Genet 16:237–251. https://doi.org/10.1038/nrg3901 View ArticlePubMedGoogle Scholar
- Neeraja CN, Maghirang-Rodriguez R, Pamplona A et al (2007) A marker-assisted backcross approach for developing submergence-tolerant rice cultivars. Theor Appl Genet 115:767–776. https://doi.org/10.1007/s00122-007-0607-0 View ArticlePubMedGoogle Scholar
- Nelissen H, Moloney M, Inzé D (2014) Translational research: from pot to plot. Plant Biotechnol J 12:277–285. https://doi.org/10.1111/pbi.12176 View ArticlePubMedGoogle Scholar
- Nelson GC, Rosegrant MR, Koo J et al (2009) Climate change: impact on agriculture and costs of adaptation. International Food Policy Research Institute, Washington, D.CGoogle Scholar
- Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017) Transcriptional regulatory network of plant heat stress response. Trends Plant Sci 22:53–65. https://doi.org/10.1016/j.tplants.2016.08.015 View ArticlePubMedGoogle Scholar
- Oka HI (1988) Origin of cultivated rice. Elsevier science publishers, AmsterdamGoogle Scholar
- Platten JD, Egdane JA, Ismail AM (2013) Salinity tolerance, Na+ exclusion and allele mining of HKT1;5 in Oryza Sativa and O. Glaberrima: many sources, many genes, one mechanism? BMC Plant Biol 13:32. https://doi.org/10.1186/1471-2229-13-32 View ArticlePubMedPubMed CentralGoogle Scholar
- Pucciariello C, Perata P (2013) Quiescence in rice submergence tolerance: an evolutionary hypothesis. Trends Plant Sci 18:377–381. https://doi.org/10.1016/j.tplants.2013.04.007 View ArticlePubMedGoogle Scholar
- Ramiah K, Ghose RLM (1951) Origin and distribution of cultivated plants of South-Asia – rice. Indian J Genet Plant Breed 11:7–13Google Scholar
- Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS One 8:e66428. https://doi.org/10.1371/journal.pone.0066428 View ArticlePubMedPubMed CentralGoogle Scholar
- Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124. https://doi.org/10.1016/j.copbio.2013.12.004 View ArticlePubMedGoogle Scholar
- Sampath S, Govindaswamy S (1958) Wild rices of Orissa and their relationship to the cultivated varieties. Rice News Teller 6:17–20Google Scholar
- Schmidhuber J, Tubiello FN (2007) Global food security under climate change. Proc Natl Acad Sci U S A 104:19703–19708. https://doi.org/10.1073/pnas.0701976104 View ArticlePubMedPubMed CentralGoogle Scholar
- Septiningsih EM, Collard BCY, Heuer S, et al (2013) Applying genomics tools for breeding submergence tolerance in Rice. In: Rajeev K V., Tuberosa R (eds) Translational genomics for crop breeding volume II: Abiotic stress, yield and quality. Chichester: Wiley, Inc, pp 9–30. https://doi.org/10.1002/9781118728482.ch2
- Shakiba E, Edwards JD, Jodari F et al (2017) Genetic architecture of cold tolerance in rice (Oryza Sativa) determined through high resolution genome-wide analysis. PLoS One 12:1–22. https://doi.org/10.1371/journal.pone.0172133 View ArticleGoogle Scholar
- Spielmeyer W, Ellis MH, Chandler PM (2002) Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proc Natl Acad Sci U S A 99:9043–9048. https://doi.org/10.1073/pnas.132266399 View ArticlePubMedPubMed CentralGoogle Scholar
- Todaka D, Shinozaki K, Yamaguchi-Shinozaki K (2015) Recent advances in the dissection of drought-stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Front Plant Sci 6:1–20. https://doi.org/10.3389/fpls.2015.00084 View ArticleGoogle Scholar
- Torres RO, McNally KL, Cruz CV et al (2013) Screening of rice Genebank germplasm for yield and selection of new drought tolerance donors. F Crop Res 147:12–22View ArticleGoogle Scholar
- Uga Y, Okuno K, Yano M (2008) QTLs underlying natural variation in stele and xylem structures of rice root. Breed Sci 58:7–14. https://doi.org/10.1270/jsbbs.58.7 View ArticleGoogle Scholar
- Uga Y, Sugimoto K, Ogawa S et al (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Genet 45:1097–1102. https://doi.org/10.1038/ng.2725 View ArticlePubMedGoogle Scholar
- UN General Assembly (2015) Transforming our world: the 2030 agenda for sustainable development. A/RES/70/1, 21 OctoberGoogle Scholar
- Vavilov NI (1926) Studies on the origin of cultivated plants. Bull Appl Bot Plant-Breeding 16:1–248Google Scholar
- Venuprasad R, Sta Cruz MT, Amante M et al (2008) Response to two cycles of divergent selection for grain yield under drought stress in four rice breeding populations. F Crop Res 107:232–244. https://doi.org/10.1016/j.fcr.2008.02.004 View ArticleGoogle Scholar
- Wheeler T, von Braun J (2013) Climate change impacts on global food security. Science 341:508–513. https://doi.org/10.1126/science.1239402 View ArticlePubMedGoogle Scholar
- Xu K, Mackill DJ (1996) A major locus for submergence tolerance mapped on rice chromosome 9. Mol Breed 2:19–224. https://doi.org/10.1007/BF00564199 Google Scholar
- Xu K, Xu X, Fukao T et al (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705–708. https://doi.org/10.1038/nature04920 View ArticlePubMedGoogle Scholar