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Mapping of QTLs for flood tolerance in rice using recombinant inbred lines of Indra and a new plant genetic resource AC 39416 A

Published online by Cambridge University Press:  22 March 2023

M. Girija Rani Open the ORCID record for M. Girija Rani [Opens in a new window] ,
P. V. Satyanarayana ,
N. Chamundeswari ,
P. V. Ramana Rao ,
M. Prabhakar ,
B. N. V. S. R. Ravikumar ,
P. Nagakumari  and
K. Kalpana
M. Girija Rani*
Affiliation:
Acharya N G Ranga Agricultural University, Regional Agricultural Research Station, Maruteru-534122, West Godavari District, AP, India
P. V. Satyanarayana
Affiliation:
Acharya N G Ranga Agricultural University, Regional Agricultural Research Station, Maruteru-534122, West Godavari District, AP, India
N. Chamundeswari
Affiliation:
Acharya N G Ranga Agricultural University, Regional Agricultural Research Station, Maruteru-534122, West Godavari District, AP, India
P. V. Ramana Rao
Affiliation:
Acharya N G Ranga Agricultural University, Regional Agricultural Research Station, Maruteru-534122, West Godavari District, AP, India
M. Prabhakar
Affiliation:
Central Institute of Dry land Agriculture, Hyderabad, Telangana, India
B. N. V. S. R. Ravikumar
Affiliation:
Acharya N G Ranga Agricultural University, Regional Agricultural Research Station, Maruteru-534122, West Godavari District, AP, India
P. Nagakumari
Affiliation:
Acharya N G Ranga Agricultural University, Regional Agricultural Research Station, Maruteru-534122, West Godavari District, AP, India
K. Kalpana
Affiliation:
Acharya N G Ranga Agricultural University, Regional Agricultural Research Station, Maruteru-534122, West Godavari District, AP, India
*
Author for correspondence: M. Girija Rani, E-mail: girijaaprri@gmail.com, m.girijarani@angrau.ac.in
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Abstract

Rice crop is affected by different types of floods at different stages of the crop cycle. Constant efforts of researchers resulted in the development of rice varieties for anaerobic germination, flash floods and stagnant flooding by both conventional and molecular breeding approaches. Detection of QTLs for different types of floods in new genetic source (AC39416A) is needed to combat adverse effects of climate change. Present investigation was carried out to identify QTLs for flood tolerance using recombinant inbred lines derived from Indra and AC39416A. QTL mapping resulted in identification of QTLs, qAG3.1 on chromosome 3 for anaerobic germination and qSF10.1 on chromosome 10 for plant survival % under stagnant flooding. These QTLs explain 59.08 and 13.21% of phenotypic variance respectively. Two candidate genes were identified in qAG3.1 region, LOC_Os03g42130 gibberellin 20 oxidase2 and LOC_Os03g44170 glutathione S-transferase. The underlying mechanism might be the inhibition of gibberellic acid synthesis and thereby protecting seedlings from oxidative stress under anoxia condition. Genomic region of qSF10.1 revealed LOC_Os10g35020 glycosyltransferase and LOC_Os10g35050 aquaporin protein loci, which might be responsible for adaptive mechanism for plant survival % under stagnant flooding. This indicates that the new genetic resource AC39416A has an ability to adopt to different types of flood tolerance in response to environmental stress. Unveiling physiological and molecular mechanisms for flood tolerance in AC39416A using advanced omics studies would help in precise genomic selections for sustained production in flood-prone areas.

Keywords

Flood tolerancelociQTL mappingriceRILs

Information

Type
Research Article
Information
Plant Genetic Resources , Volume 20 , Issue 4 , August 2022 , pp. 270 - 276
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press on behalf of NIAB

Introduction

Rice is an important staple food crop for more than half of the world's population. Rice productivity has to be improved enormously to meet the demands of growing population. Rice farmers in flood-prone ecosystem are more vulnerable to changing climatic conditions and constitute about 7% of global rice area (Yang et al., Reference Yang, Wu, Chen, Lai, Yen and Yang2017). Enhancing rice productivity in marginal environments is essential to improve the livelihood of the farming community (Panda and Barik, Reference Panda and Barik2021). Rice crop suffers four major types of floods from seed germination to harvesting stage: (a) anaerobic germination, where submergence happens during germination, (b) flash floods where plants are completely submerged for 2 weeks, (c) stagnant flooding (SF) with up to 30–50 cm deep water due to prolonged floods and (d) deep water ecology with water depth more than 50 cm for most of time (Mackill et al., Reference Mackill, Ismail, Pamplona, Sanchez, Carandang and Septiningsih2010). Submergence up to 50% plant height at any growth stage leads to reduction of rice yield by at least 25% (Swain et al., Reference Swain, Herath, Pathirana and Mittra2005) and yield loss up to 47% under SF (Kato et al., Reference Kato, Collard, Septiningsih and Ismail2014). Two major adaptive mechanisms for flood tolerance are quiescence and escape.

Anaerobic germination is prerequisite not only for rice cultivation under direct seeded condition but also required for survival of crop at nursery stage in flood-prone lowland areas during monsoon. Multiple QTLs for anaerobic germination qAG-1, qAG-2, qAG-7, qAG-5a and qAG-5b (Ling et al., Reference Ling, Ming-yu, Ming and Jian-min2004), qAG-1, qAG-2-1, qAG-11 and qAG-12 from KHAIYAN (Angaji, Reference Angaji2008), qAG-1-2, qAG-3-1, qAG-7-2, qAG-9-1, qAG-9-2 using Khao Hlan (Angaji et al., Reference Angaji, Septiningsih, Mackill and Ismail2010), a large QTL on chromosome 7 from Mazhan Red (Septiningsih et al., Reference Septiningsih, Ignacio, Sendon, Sanchez, Ismail and Mackill2013) and qAG7 from Nanhi (Baltazar et al., Reference Baltazar, Ignacio, Thomson, Ismail and Septiningsih2014) were identified. One major QTL on AG1 was incorporated in Chierangsub1 (Toledo et al., Reference Toledo, Ignacio, Casal, Gonzaga, Mendioro and Septiningsih2015).

Flash flood tolerance conferring Sub1A, an ethylene-responsive factor gene, was identified from FR 13 A (Xu et al., Reference Xu, Xia, Fukao, Canlas, Maghirang-Rodriguez, Heuer, Ismail, Bailey-Serres, Ronald and Mackill2006). This Sub1A gene was widely exploited by incorporating it into popular rice varieties globally (Neeraja et al., Reference Neeraja, Maghirang Rodriguez, Pamplona, Heuer, Collard, Septiningsih, Vergara, Sanchez, Xu, Ismail and Mackill2007; Septiningsih et al., Reference Septiningsih, Pamplona, Sanchez, Neeraja, Vergara, Heuer, Ismail and Mackill2009, Reference Septiningsih, Hidayatun, Sanchez, Nugraha, Carandang, Pamplona, Collard, Ismail and Mackill2014; Khanh et al., Reference Khanh, Linh, Linh, Ham and Xuan2013; Nawarathna et al., Reference Nawarathna, Perera and Samarasinghe2014; Ara et al., Reference Ara, Uddin, Iftekharuddaula, Saikat and Khan2015; Girijarani et al., Reference Girijarani, Satyanarayana, Suryanarayana, Ramanarao, Neerajakshi, Chamundeswari, Ravikumar, Pavani, Kondayya, Ratnasree, Vishnuvardhan, Sivaramprasad and Reddy2015; Iftekharuddaula et al., Reference Iftekharuddaula, Ahmed, Ghosal, Moni, Amin and Ali2015, Reference Iftekharuddaula, Ahmed, Ghosal, Amin, Moni, Bisnu, Hirendra, Siddiquea, Collard and Septiningsih2016; Singh et al., Reference Singh, Singh, Xalaxo, Verulkar, Yadav, Singh, Singh, Prasad, Kondayya, Ramana Rao, Girija Rani, Anuradha, Suraynarayana, Sharma, Krishnamurthy, Sharma, Dwivedi, Singh, Singh, Nilanjay, Singh, Kumar, Chetiah, Ahmad, Rai, Perraju, Anita, Singh, Mandal, Reddy, Singh, Katara, Marandi, Swain, Sarkar, Singh, Mohapatra, Padmawathi, Ram, Kathiresan, Paramsivam, Nadarajan, Thirumeni, Nagarajan, Singh, Vikram, Kumar, Septiningshih, Singh, Ismail, Mackill and Singh2016; Ahmed et al., Reference Ahmed, Rafii, Ismail, Abdul, Rahim, Tanweer and Latif2016; Korinsak et al., Reference Korinsak, Siangliw, Kotcharerk, Jirapong, Jonaliza, Boonrat, Grienggrai, Nitat and Theerayut2016; Aditi et al., Reference Aditi, Pawan, Neera, Renu, Yashi, Balwant, Nisha, Sangeeta, Amitha, Vandna, Satish, Ramana Rao, Girija Rani, Anuradha, Satyanarayana, Krishnamurthy, Prabodh, Deepika Singh, Nilanjay, Kumar, Sanjay, Ahmad, Mayank, Jawahar, Marandi, Padmini, Sarkar, Singh, Reddy, Nimai, Paramsivam, Nadarajan, Thirumeni, Jyothi, Padmavathi, Ram and Singh2019). Three non-Sub1 QTLs were identified from IR 72 (Septiningsih et al., Reference Septiningsih, Sanchez, Singh, Sendon, Pamplona, Heuer and Mackill2012), three from FR 13A on chromosomes 1, 8 and 10 (Gonzaga et al., Reference Gonzaga, Carandang, Sanchez, Mackill and Septiningsih2016) and a major QTL for submergence qSUB8.1 from Ciherang Sub1 (Gonzaga et al., Reference Gonzaga, Carandang, Anshuman, Collard, Thomson and Septiningsih2017).

Most of the Sub1 incorporated lines are vulnerable to survive under SF (Sarkar and Bhattacharjee, Reference Sarkar and Bhattacharjee2011; Sandhya Rani et al., Reference Sandhya Rani, Kutubuddin, Chattopadhyay, Sarkar and Pravat Kumar2019). Survival per cent and yield under SF are dependent on moderate elongation, high tillering, lesser carbohydrate depletion and higher fertility (Vergara et al., Reference Vergara, Nugraha, Esguerra, Mackill and Ismail2014). QTLs for grain yield under SF, along with days to flowering, flag leaf length and leaf sheath length, were detected by Singh et al. (Reference Singh, Carandang, Gonzaga, Collard, Ismail and Septiningsih2017a, Reference Singh, Septiningsih, Balyan, Singh and Rai2017b). Existence of compensatory mechanisms between tiller growth and shoot elongation under SF results in poor yields in addition to lodging risk (Zhu et al., Reference Zhu, Chen, Ella and Ismail2018). Land races tolerating flash floods and SF were assessed for genetic diversity (Barik et al., Reference Barik, Kumar, Lenka and Panda2020). Genetic resources like AC37887 and AC39416A that can tolerate anaerobic germination and SF were identified by Sandhya et al. (Reference Sandhya, Kuanar, Ray, Sethi, Chattopadhyay and Sarkar2017).

Submergence-tolerant varieties with the Sub1 gene do not usually possess traits for anaerobic germination and SF indicating that the genes governing these traits are independent to Sub1. QTL mapping and candidate gene discovery from new genetic resources that have excellent adaptation to different kinds of flooding is very important for breeding climate-resilient flood-tolerant rice varieties (Singh et al., Reference Singh, Carandang, Gonzaga, Collard, Ismail and Septiningsih2017a, Reference Singh, Septiningsih, Balyan, Singh and Rai2017b).

The present study is designed to identify QTLs for flood tolerance using 184 recombinant inbred lines (RILs) developed using Indra (MTU 1061) as female parent and new genetic resource AC 39416A for anaerobic germination and SF.

Materials and methods

Development of RILs

Indra (MTU 1061), a high yielding popular rice variety, was developed by crossing PLA 1100 and MTU 1010 and was released in 2006 by Regional Agricultural Research Station (RARS), Maruteru of Acharya NG Ranga Agricultural University (ANGRAU). Indra variety that is tolerant to flash floods for 1 week and susceptible to anaerobic germination and SF (Girijarani et al., Reference Girijarani, Suryanarayana, Satyanarayana, Ramana Rao, Prasad, Neerajakshi, Chamundeswari and Ravikumar2013; Reddy et al., Reference Reddy, Girija Rani, Satyanarayana, Suryanarayana, Chamundeswari, Ravi Kumar, Ramana Rao and Vishnuvardhan2015) was used as female parent. New genetic resource AC39416A collected from National Rice Research Institute (NRRI), Cuttack was used as donor. AC39416A can tolerate 3 weeks of anaerobic germination and SF (Sandhya et al., Reference Sandhya, Kuanar, Ray, Sethi, Chattopadhyay and Sarkar2017). Cross was initiated during wet season of 2013 and 4000 plants were obtained in F2 generation. One hundred eighty-four single plants from F2 population were randomly selected and advanced up to F6 generation by single seed descent method at RARS, Maruteru during 2014–2016.

Genotyping of RILs

Genomic DNA was isolated using the method of Zheng et al. (Reference Zheng, Subudhi, Domingo, Magantay and Huang1995). Quality and quantity were estimated using eight channel vis spectrophotometer (Thermo scientific, USA). Polymerase chain reaction mixture of 10 μl comprising of 10 ×  Taq buffer A 1 μl, forward and reverse primer each 1 μl (Sigma aldirch), 2.5 mm dntp 0.5 μl (Genei), one unit of Taq DNA polymerase 1 μl (Genei), 25 ng of genomic DNA 3 μl and sterile distilled water 2.5 μl was used for amplification. Thermo profile of initial denaturation at 94°C for 5 min followed by 35 cycles of denaturing at 94°C for 30 s, annealing at 55°C for 0.5 min, extension at 72°C for 1.0 min and ending up with 7 min at 72°C for the final extension was adopted using Pro S master cycler (Eppendorf). Electrophoresis was carried out on 3% agarose gels and images were visualized using Syngene gel documentation system.

Out of 624 markers screened for parental polymorphism between Indra and AC 39416 A at RARS, Maruteru, 104 polymorphic simple sequence repeats markers were used to genotype 184 RILs. Saturated fine mapping was performed using more markers within the identified QTL regions. Five polymorphic markers were identified between RM15848 and RM15561 for qAG3.1 and six for qSF10.1 between RM 304 and RM 6100 for fine mapping. Gel images were scored as A for Indra allele, B for AC 39416A allele and H for heterozygote. QTL mapping was performed using QCIM software with 1000 permutations as per Wang et al. (Reference Wang, Li, Zhang and Meng2016).

Phenotyping of RILs

Anaerobic germination (AG)

For each RIL, 30 pre germinated seeds were sowed on third day in pro trays. These trays were submerged in a concrete tank by maintaining 10 cm deep for 3 weeks during 2016 and 2017 (Fig. 1(a)–(c)). Survived plants after 21 days were counted for anaerobic germination.

Fig. 1.

Phenotypic screening of RILs for anaerobic germination and SF.

Stagnant flooding (SF)

Thirty-day-old seedlings of RILs were transplanted in submergence pond with a spacing of 20 cm between rows and 15 cm between plants with 25 hills per row. Water depth of 30–50 cm was maintained from 1 week after transplanting to reproductive phase during 2017 and 2018 (Fig. 1(d)). Survived plants were counted at 30 days after transplanting. Plant survival % was calculated as number of (plants survived/total number of plants) × 100.

Fig. 2.

Frequency distribution of 184 RILs for plant survival % under anaerobic germination and SF.

Results

Plant survival % for anaerobic germination shows a wide variation (0–90%) even under SF (0–100%) (Table 1). Majority of RILs have an anaerobic germination per cent ranging between 40 and 60% with a mean of 43.32. Similarly, plant survival under SF is on the lower end of distribution with a mean of 26.93% (Fig. 2). Only four RILs for anaerobic germination and six RILs under SF show maximum plant survival %, with a range between 81 and 100%. Only one RIL has a maximum performance with about 70% plant survival rate under AG and 100% under SF. Parent AC 39416 A has a higher plant survival rate of 88.80% under anaerobic condition and 78.69% under SF than the check Swarnasub1 (34.30% AG, 20.20% SF) and female parent Indra (10% AG, 16.67% SF).

Fig. 3.

QTL for Anaerobic germination qAG 3.1on Chromosome 3.

Table 1.

Summary of anaerobic germination and plant survival % under stagnant flooding among RILs

Results of QTL mapping revealed that QTLs for anaerobic germination qAG3.1 were found on chromosome 3 between RM 15848 (24.68 Mbp) and RM 15561 (24.82 Mbp) with a LOD score of 2.89. The phenotypic variation explained is about 7.16% with an additive effect of 4.48 (Table 2). Fine mapping of qAG 3.1 resulted in identification of a major QTL with LOD score of 5.36 that explains a phenotypic variance of 59.08%. This QTL is between RM 15554 (24.72 Mbp) and RM 15561 (24.82 Mbp) (Fig. 3). The identified QTL qAG3.1 was also validated in another population consisting of BC1F1 lines of Swarnasub1 and AC 39416 A that was developed under NICRA project during 2018.

Table 2.

Identified QTLs for flood tolerance using RILs of AC39416A

QTL for plant survival % under SF qSF10.1 was detected on chromosome 10 with a LOD score of 5.66, a phenotypic variance of 13.21% and an additive effect of 10.79. The identified QTL for SF qSF10.1 was validated in the year 2018 by screening RILs under SF with a LOD score of 3.10, phenotypic variance of 7.56 and an additive effect of 7.71 between RM 304 (18.65 Mbp) and RM 6737 (18.71 Mbp) represented in Fig. 4 and Table 2.

Fig. 4.

QTL qSF10.1 for plant survival % under stagnant flooding.

Rice gene annotation (http://rice.plantbiology.msu.edu/) revealed LOC_Os03g42130 gibberellin 20 oxidase2 and LOC_Os03g44170 glutathione S-transferase as putative candidate gene loci that might be responsible for anaerobic germination in our identified QTL qAG 3.1 genomic region on chromosome 3. The genomic region of QTL for plant survival %, qSF10.1 revealed LOC_Os10g35020 glycosyltransferase and LOC_Os10g35050 aquaporin proteins as putative candidate genes that play a role for plant survival % under SF.

Discussion

Variation in RILs for anaerobic germination and plant survival % under SF indicated that expression of alleles for different types of floods is different and it depends on plant adaptive mechanism in response to stress signalling. Rice plant coleoptile has to grow faster under anoxia for germination and show moderate elongation under SF. In the present study too, only one RIL was detected as tolerant for both situations and AC39416A has significantly higher plant survival % than Swarnasub1 and Indra. Rumanti et al. (Reference Rumanti, Sitaresmi and Nugraha2022) and Agbeleye et al. (Reference Agbeleye, Olubiyi, Ehirim, Shittu, Jolayemi, Adetimirin, Ariyo, Sanni and Venuprasad2019) also found significant variation in plant survival % for both AG and SF and identified different tolerant accessions for each.

QTLs for anaerobic germination qAG 3.1 on chromosome 3 and qSF10.1 for plant survival % under SF on chromosome 10 were detected using RILs of Indra and AC 39416A. This indicated that alleles contributing to different types of floods are present in AC39416A.

Angaji et al. (Reference Angaji, Septiningsih, Mackill and Ismail2010) also reported QTL for anaerobic germination qAG 3 between RM 7094 (26.87 Mbp) and RM 520 (30.91 Mbp) on chromosome 3 using Khao Hlan On as donor, RILs of Nampyeong/PBR cross (Jeong et al., Reference Jeong, Cho and Jeong2020), F2:3 population of Nanhi/IR64 (Baltazar et al., Reference Baltazar, Ignacio, Thomson, Ismail and Septiningsih2014) and IR64/Kharsu 80A (Baltazar et al., Reference Baltazar, Ignacio, Thomson, Ismail, Mendioro and Septiningsih2019). The above results support the idea that QTL qAG3.1 possesses genes that trigger signals for anaerobic germination from AC39416A.

Identified QTL for plant survival % under SF is in the vicinity of a reported QTL for plant survival on chromosome 10 between RM 222 (20.70 Mbp) and qSUB10.1 at RM25835 (21.31 Mb; Gonzaga et al., Reference Gonzaga, Carandang, Sanchez, Mackill and Septiningsih2016). QTLs for plant survial % (Toojinda et al., Reference Toojinda, Siangliw, Tragoonrung and Vanavichit2003) in F2 derived population of Jao Him Nin/KDML 105, grain weight and days to 50% flowering under SF were also identified on chromosome 10 in RILs of Ciherang-Sub1/IR10F365 (Singh et al., Reference Singh, Carandang, Gonzaga, Collard, Ismail and Septiningsih2017a, Reference Singh, Septiningsih, Balyan, Singh and Rai2017b) and Swarna/Rashpanjor (Chattopadhyay et al., Reference Chattopadhyay, Chakraborty, Samal and Sarkar2021).

LOC_Os03g42130 gibberellin 20 oxidase2, a putative gene locus, inhibits gibberellic acid biosynthesis under anoxia conditions. Production of α-amylase does not require gibberellic acid for germination under anaerobic conditions (Loreti et al., Reference Loreti, Yamaguchi, Alpi and Perata2003) and the amylase activity remained unchanged under anaerobic germination in AC39416A and FR 13A (Sweetaleena et al., Reference Sweetaleena, Sandhay Rani and Sarkar2019). LOC_Os03g44170 glutathione S-transferase, a putative candidate gene locus, might also play a role in crosstalk between submergence tolerance during germination (Thapa et al., Reference Thapa, Tabien, Thomson and Septiningsih2022) and hormone response pathways (Jain et al., Reference Jain, Ghanashyam and Annapurna2010), and also protects the plants from oxidative stress under anoxia conditions (Kumar and Trivedi, Reference Kumar and Trivedi2018).

Results of gene prediction between RM 304 (18.650 Mbp) and RM 6737 (18.71 Mbp) revealed putative candidate gene LOC_Os10g35020 glycosyltransferase and LOC_Os10g35050 aquaporin protein that might be responsible for plant survival % under SF. Glycosyltransferase plays a role in antioxidant defence mechanism under flooding (Sanhezz-Bermudez et al., Reference Sanhez-Bermudez, del Pozo and Pernas2022) and submergence tolerance on chromosome 10 (Qi et al., Reference Qi, Kawano, Yamauchi, Ling, Li and Tanaka2005) by expression of genes with response to ethylene and gibberellin. LOC_Os10g35050 aquaporin protein putative candidate genes also play a role in adaptive mechanism for plant survival % under SF. Partial to prolonged SF might have triggered protein accumulation of aquaporins (Tyerman et al., Reference Tyerman, Niemietz and Bramley2002). Plant aquaporin not only play a role to facilitate osmotic water transport across membranes but also transports nutrients like urea (Gaspar et al., Reference Gaspar, Bousser, Sissoëff, Roche, Hoarau and Mahé2003), ammonia (Loque et al., Reference Loque, Ludewig, Yuan and Von Wirén2005) and CO2 (Hanba et al., Reference Hanba, Shibasaka, Hayashi, Hayakawa, Kasamo, Terashima and Katsuhara2004). The presence of glycosyltransferase loci might trigger hormone response pathways for plant survival % and aquaporin proteins loci might manifest the plant for nutrient uptake and gas diffusion for adaptation under SF.

Conclusion

In this study, identified QTLs qAG 3.1 for anaerobic germination for 21 days and qSF10.1 for plant survival % under SF from RILs generated by Indra/AC39416A can be further exploited for marker-assisted gene pyramiding using AC 39416A as donor for both anaerobic germination and SF. Studies on gene prediction revealed that AC39416 A adapts to anaerobic germination and SF by constitutive protein production in response to particular environmental signalling which has to be further traced out by advanced physiological and molecular studies.

Acknowledgements

We acknowledge the National Initiative for climatic resilience in Agriculture (NICRA) for providing funds under sponsored grant to carryout above research work at the Regional Agricultural Research Station, Maruteru of Acharya NG Ranga Agricultural University, Andhra Pradesh, India. We acknowledge Dr Sujan Mamidi for editing the manuscript.

Conflict of interest

None.

References

Aditi, B, Pawan, J, Neera, Y, Renu, S, Yashi, S, Balwant, S, Nisha, S, Sangeeta, S, Amitha, S, Vandna, R, Satish, V, Ramana Rao, PV, Girija Rani, M, Anuradha, T, Satyanarayana, PV, Krishnamurthy, SL, Prabodh, S, Deepika Singh, PK, Nilanjay, , Kumar, R, Sanjay, Ch, Ahmad, T, Mayank, R, Jawahar, K, Marandi, B, Padmini, S, Sarkar, RK, Singh, DP, Reddy, JN, Nimai, M, Paramsivam, K, Nadarajan, S, Thirumeni, S, Jyothi, B, Padmavathi, G, Ram, T and Singh, NK (2019) Genomics-assisted backcross breeding for infusing climate resilience in high-yielding green revolution varieties of rice. Indian Journal of Genetics and Plant Breeding 79 (Suppl), 160–170.Google Scholar
Agbeleye, OA, Olubiyi, MR, Ehirim, BO, Shittu, AO, Jolayemi, OL, Adetimirin, VO, Ariyo, OJ, Sanni, KA and Venuprasad, R (2019) Screening African rice (O. glaberrima Steud.) for tolerance to abiotic stress III Flooding. SABRAO Journal of Breeding and Genetics 51, 128–150.Google Scholar
Ahmed, F, Rafii, MY, Ismail, MZ, Abdul, SJ, Rahim, HA, Tanweer, FA and Latif, MA (2016) Recurrent parent genome recovery in different populations with the introgression of Sub1 gene from a cross between MR219 and Swarna-Sub1. Euphytica 207, 605–618.10.1007/s10681-015-1554-5CrossRefGoogle Scholar
Angaji, SA (2008) Mapping QTLs for submergence tolerance during germination in rice. African Journal of Biotechnology 7, 2551–2558.Google Scholar
Angaji, S, Septiningsih, EM, Mackill, DJ and Ismail, AM (2010) QTLs associated with tolerance of anaerobic conditions during germination in rice (Oryza sativa L.). Euphytica 172, 159–168.10.1007/s10681-009-0014-5CrossRefGoogle Scholar
Ara, A, Uddin, ABMA, Iftekharuddaula, KM, Saikat, MMH and Khan, MAI (2015) Introgression of Sub1 QTL into a rainfed lowland rice variety of Bangladesh using marker-assisted backcross approach. International Journal of Research 2, 233–244.Google Scholar
Baltazar, MD, Ignacio, JCI, Thomson, MJ, Ismail, AM and Septiningsih, EM (2014) QTL mapping for tolerance of anaerobic germination from IR64 and the aus landrace Nanhi using SNP genotyping. Euphytica 197, 251–260.10.1007/s10681-014-1064-xCrossRefGoogle Scholar
Baltazar, MD, Ignacio, JCI, Thomson, MJ, Ismail, AM, Mendioro, MS and Septiningsih, EM (2019) QTL mapping for tolerance to anaerobic germination in rice from IR64 and the aus landrace Kharsu 80A. Breeding Science 69, 227–233.10.1270/jsbbs.18159CrossRefGoogle ScholarPubMed
Barik, J, Kumar, V, Lenka, SK and Panda, D (2020) An assessment of variation in morpho-physiological traits and genetic diversity in relation to submergence tolerance of five indigenous landraces of lowland rice. Rice Science 27, 32–43.CrossRefGoogle Scholar
Chattopadhyay, K, Chakraborty, K, Samal, P and Sarkar, RK (2021) Identification of QTLs for stagnant flooding tolerance in rice employing genotyping by sequencing of a RIL population derived from Swarna × Rashpanjor. Physiology and Molecular Biology of Plants 27, 2893–2909.10.1007/s12298-021-01107-xCrossRefGoogle ScholarPubMed
Gaspar, M, Bousser, A, Sissoëff, I, Roche, O, Hoarau, J and Mahé, A (2003) Cloning and characterization of ZmPIP1-5b, an aquaporin transporting water and urea. Plant Science 165, 21–31.10.1016/S0168-9452(03)00117-1CrossRefGoogle Scholar
Girijarani, M, Suryanarayana, Y, Satyanarayana, PV, Ramana Rao, PV, Prasad, KSN, Neerajakshi, Ch, Chamundeswari, N and Ravikumar, BNVSR (2013) Screening of rice genotypes for anaerobic germination. In Extended Summaries of ARRW Golden Jubilee International Symposium, India: Cuttack, p. 240.Google Scholar
Girijarani, M, Satyanarayana, PV, Suryanarayana, Y, Ramanarao, PV, Neerajakshi, C, Chamundeswari, N, Ravikumar, BNSVR, Pavani, SL, Kondayya, K, Ratnasree, P, Vishnuvardhan, KM, Sivaramprasad, K and Reddy, AV (2015) Enhancement of flood tolerance in a high yielding rice variety ‘Amara’ by marker assisted selection. SABRAO Journal of Breeding Genetics 47, 439–447.Google Scholar
Gonzaga, ZJ, Carandang, J, Sanchez, DL, Mackill, DJ and Septiningsih, EM (2016) Mapping additional QTLs from FR13A to increase submergence tolerance beyond SUB1. Euphytica 209, 627–636.10.1007/s10681-016-1636-zCrossRefGoogle Scholar
Gonzaga, ZJ, Carandang, J, Anshuman, S, Collard, BCY, Thomson, MJ and Septiningsih, EM (2017) Mapping QTLs for submergence tolerance in rice using a population fixed for SUB1A tolerant allele. Molecular Breeding 37, 47.10.1007/s11032-017-0637-5CrossRefGoogle Scholar
Hanba, YT, Shibasaka, M, Hayashi, Y, Hayakawa, T, Kasamo, K, Terashima, I and Katsuhara, M (2004) Overexpression of the barley aquaporin HvPIP2;1 increases internal CO2 conductance and CO2 assimilation in the leaves of transgenic rice plants. Plant Cell Physiology 45, 521–529.10.1093/pcp/pch070CrossRefGoogle ScholarPubMed
Iftekharuddaula, KM, Ahmed, HU, Ghosal, S, Moni, ZH, Amin, A and Ali, MD (2015) Development of new submergence tolerant rice variety for Bangladesh using marker-assisted backcrossing. Rice Science 22, 16–26.10.1016/j.rsci.2015.05.003CrossRefGoogle Scholar
Iftekharuddaula, KM, Ahmed, HU, Ghosal, S, Amin, A, Moni, ZR, Bisnu, PR, Hirendra, NB, Siddiquea, MA, Collard, BCY and Septiningsih, EM (2016) Development of early maturing submergence-tolerant rice varieties for Bangladesh. Field Crop Research 6594, 10.Google Scholar
Jain, M, Ghanashyam, C and Annapurna, B (2010) Comprehensive expression analysis suggests overlapping and specific roles of rice glutathione S-transferase genes during development and stress responses. BMC Genomics 11, 73.10.1186/1471-2164-11-73CrossRefGoogle ScholarPubMed
Jeong, JM, Cho, YC and Jeong, JU (2020) QTL mapping and effect confirmation for anaerobic germination tolerance derived from the japonica weedy rice landrace PBR. Plant Breeding 139, 83–92.10.1111/pbr.12753CrossRefGoogle Scholar
Kato, Y, Collard, BCY, Septiningsih, EM and Ismail, AM (2014) Physiological analyses of traits associated with tolerance of long-term partial submergence in rice. AoB Plants 6, plu058.10.1093/aobpla/plu058CrossRefGoogle ScholarPubMed
Khanh, TD, Linh, LH, Linh, TH, Ham, LH and Xuan, TD (2013) Rapid and high-precision marker assisted backcrossing to introgress the SUB1 QTL into the Vietnamese elite rice variety. Journal of Plant Breeding Crop Science 5, 26–33.10.5897/JPBCS12.052CrossRefGoogle Scholar
Korinsak, S, Siangliw, M, Kotcharerk, J, Jirapong, J, Jonaliza, LS, Boonrat, J, Grienggrai, P, Nitat, S and Theerayut, T (2016) Improvement of the submergence tolerance and the brown planthopper resistance of the Thai jasmine rice cultivar KDML105 by pyramiding Sub1 and Qbph12. Field Crop Research 188, 105–112.10.1016/j.fcr.2015.10.025CrossRefGoogle Scholar
Kumar, S and Trivedi, PK (2018) Glutathione S-transferases: role in combating abiotic stresses including arsenic detoxification in plants. Frontiers in Plant Science 9, 1–9. Available at https://doi.org/10.3389/fpls.2018.00751CrossRefGoogle ScholarPubMed
Ling, J, Ming-yu, HW, Ming, C and Jian-min, W (2004) Quantitative trait loci and epistatic analysis of seed anoxia germinability in rice (Oryza sativa L.). Rice Science 11, 238–244.Google Scholar
Loque, D, Ludewig, U, Yuan, L and Von Wirén, N (2005) Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiology 137, 671–680.10.1104/pp.104.051268CrossRefGoogle ScholarPubMed
Loreti, E, Yamaguchi, J, Alpi, A and Perata, P (2003) Gibberellins are not required for rice germination under anoxia. Plant and Soil 253, 137–143.10.1023/A:1024539011641CrossRefGoogle Scholar
Mackill, DJ, Ismail, AM, Pamplona, AM, Sanchez, DL, Carandang, JJ and Septiningsih, EM (2010) Stress tolerant rice varieties for adaptation to a changing climate. Crop Environment & Bioinformatics 7, 250–259.Google Scholar
Nawarathna, RN, Perera, ALT and Samarasinghe, WLG (2014) Screening of BC1F1 population (BG 379-2/IR 07F102//BG 379-2) of rice (Oryza sativa L.) for submergence tolerance using molecular markers. Journal of Agricultural Sciences 9, 147–153.10.4038/jas.v9i3.7437CrossRefGoogle Scholar
Neeraja, CN, Maghirang Rodriguez, R, Pamplona, A, Heuer, S, Collard, BC, Septiningsih, EM, Vergara, G, Sanchez, D, Xu, K, Ismail, AM and Mackill, DJ (2007) A marker-assisted backcross approach for developing submergence-tolerant rice cultivars. Theoretical Applied Genetics 115, 767–776.10.1007/s00122-007-0607-0CrossRefGoogle ScholarPubMed
Panda, D and Barik, J (2021) Flooding tolerance in rice: focus on mechanisms and approaches. Rice Science 28, 43–47.10.1016/j.rsci.2020.11.006CrossRefGoogle Scholar
Qi, Y, Kawano, N, Yamauchi, Y, Ling, J, Li, D and Tanaka, K (2005) Identification and cloning of a submergence-induced gene OsGGT (glycogenin glucosyltransferase) from rice (Oryza sativa L.) by suppression subtractive hybridization. Planta 221, 437–445.CrossRefGoogle ScholarPubMed
Reddy, AV, Girija Rani, M, Satyanarayana, PV, Suryanarayana, Y, Chamundeswari, N, Ravi Kumar, BNVSR, Ramana Rao, PV and Vishnuvardhan, KM (2015) Physiological and molecular response of rice genotypes for different types of flooding. Current Biotica 8, 345–350.Google Scholar
Rumanti, A, Sitaresmi, T and Nugraha, Y (2022) Rice tolerance variation to long-term stagnant flooding and germination ability under an-aerobic. IOP Conference Series: Earth Environmental Science 423, 012048.Google Scholar
Sandhya, R, Kuanar, A, Ray, S, Sethi, K, Chattopadhyay, K and Sarkar, RK (2017) Physiological basis of stagnant flooding tolerance in rice. Rice 24, 73–84.Google Scholar
Sandhya Rani, K, Kutubuddin, AM, Chattopadhyay, K, Sarkar, RK and Pravat Kumar, M (2019) Introgression of Sub1 (SUB1) QTL in mega rice cultivars increases ethylene production to the detriment of grain- filling under stagnant flooding. Scientific Reports 9, 18567.Google Scholar
Sanhez-Bermudez, M, del Pozo, JC and Pernas, M (2022) Effects of combined abiotic stresses related to climate change on root growth in crops. Frontiers in Plant Science 13, 918537.CrossRefGoogle Scholar
Sarkar, RK and Bhattacharjee, B (2011) Rice genotypes with Sub1 QTL differ in submergence tolerance, elongation ability during sub- mergence, and re-generation growth at re-emergence. Rice 5, 7.CrossRefGoogle Scholar
Septiningsih, EM, Pamplona, AM, Sanchez, DL, Neeraja, CN, Vergara, GV, Heuer, S, Ismail, AM and Mackill, DJ (2009) Development of submergence-tolerant rice cultivars: the Sub1 locus and beyond. Annals of Botany 103, 151–160.CrossRefGoogle ScholarPubMed
Septiningsih, EM, Sanchez, DL, Singh, N, Sendon, PMD, Pamplona, AM, Heuer, S and Mackill, DJ (2012) Identifying novel QTLs for submergence tolerance in rice cultivars IR72 and Madabaru. Theoretical and Applied Genetics 124, 867–874.CrossRefGoogle ScholarPubMed
Septiningsih, EM, Ignacio, JCI, Sendon, PMD, Sanchez, DL, Ismail, AM and Mackill, DJ (2013) QTL mapping and confirmation for tolerance of anaerobic conditions during germination derived from the rice landrace Ma-Zhan Red. Theoretical and Applied Genetics 126, 1357–1366.CrossRefGoogle ScholarPubMed
Septiningsih, EM, Hidayatun, N, Sanchez, DL, Nugraha, Y, Carandang, J, Pamplona, AM, Collard, BCY, Ismail, AM and Mackill, DJ (2014) Accelerating the development of new submergence tolerant rice varieties: the case of Ciherang-Sub1 and PSB Rc18-Sub1. Euphytica 202, 259–268.CrossRefGoogle Scholar
Singh, R, Singh, Y, Xalaxo, S, Verulkar, S, Yadav, N, Singh, S, Singh, N, Prasad, KSN, Kondayya, K, Ramana Rao, PV, Girija Rani, M, Anuradha, T, Suraynarayana, Y, Sharma, PC, Krishnamurthy, SL, Sharma, SK, Dwivedi, JL, Singh, AK, Singh, PK, Nilanjay, , Singh, NK, Kumar, R, Chetiah, SK, Ahmad, T, Rai, M, Perraju, P, Anita, P, Singh, DN, Mandal, NP, Reddy, JN, Singh, ON, Katara, JL, Marandi, B, Swain, P, Sarkar, RK, Singh, DP, Mohapatra, , Padmawathi, G, Ram, T, Kathiresan, RM, Paramsivam, K, Nadarajan, S, Thirumeni, S, Nagarajan, M, Singh, AK, Vikram, P, Kumar, A, Septiningshih, E, Singh, US, Ismail, AM, Mackill, D and Singh, NK (2016) From QTL to variety-harnessing the benefits of QTLs for drought, flood and salt tolerance in mega rice varieties of India through a multi-institutional network. Plant Science 242, 278–287.CrossRefGoogle ScholarPubMed
Singh, A, Carandang, J, Gonzaga, ZJC, Collard, BCY, Ismail, AM and Septiningsih, EM (2017 a) Identification of QTLs for yield and agronomic traits in rice under stagnant flooding conditions. Rice 10, 15.CrossRefGoogle ScholarPubMed
Singh, A, Septiningsih, EM, Balyan, HS, Singh, NK and Rai, V (2017 b) Genetics, physiological mechanisms and breeding of flood-tolerant rice (Oryza sativa L.). Plant Cell Physiology 58, 185–197.Google ScholarPubMed
Swain, DK, Herath, S, Pathirana, A and Mittra, BN (2005) Rainfed lowland and flood prone rice: a critical review on ecology and management technology for improving the productivity in Asia. In Role of Water Sciences in Transboundary River Basin Management, Thailand.Google Scholar
Sweetaleena, S, Sandhay Rani, K and Sarkar, RK (2019) Anaerobic germination potential in rice (Oryza sativa L.): role of amylases, alcohol dehydrogenase and ethylene. Journal of Stress Physiology & Biochemistry 15, 39–52.Google Scholar
Thapa, R, Tabien, RE, Thomson, MJ and Septiningsih, EM (2022) Genetic factors underlying anaerobic germination in rice: genome-wide association study and transcriptomic analysis. The Plant Genome, e20261. Available at https://doi.org/10.1002/tpg2.20261.CrossRefGoogle ScholarPubMed
Toledo, AM, Ignacio, JCI, Casal, C, Gonzaga, ZJ, Mendioro, MS and Septiningsih, EM (2015) Development of improved Ciherang-Sub1 having tolerance to anaerobic germination conditions. Plant Breeding Biotechnology 3, 77–87.CrossRefGoogle Scholar
Toojinda, T, Siangliw, M, Tragoonrung, S and Vanavichit, A (2003) Thai Jasmine rice carrying QTLCh9 (Sub1 QTL) is submergence tolerant. Annals of Botany 91, 225–261.Google Scholar
Tyerman, SD, Niemietz, CM and Bramley, H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environment 25, 173–194.CrossRefGoogle ScholarPubMed
Vergara, GV, Nugraha, Y, Esguerra, MQ, Mackill, DJ and Ismail, AM (2014) Variation in tolerance of rice to long-term stagnant flooding that submerges most of the shoot will aid in breeding tolerant cultivars. AoB PLANTS 6, plu055. doi: 10.1093/aobpla/plu055CrossRefGoogle ScholarPubMed
Wang, J, Li, H, Zhang, L and Meng, L (2016) User's Manual of QTL IciMapping. China: The Quantitative Genetics Group, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS), Mexico: Genetic Resources Program, International Maize and Wheat Improvement Center (CIMMYT).Google Scholar
Xu, K, Xia, X, Fukao, T, Canlas, P, Maghirang-Rodriguez, R, Heuer, S, Ismail, AI, Bailey-Serres, J, Ronald, PC and Mackill, DJ (2006) Sub1A is an ethylene response factor-like gene that confers submergence tolerance to rice. Nature 442, 705–708.CrossRefGoogle ScholarPubMed
Yang, SY, Wu, YS, Chen, CT, Lai, MH, Yen, HM and Yang, CY (2017) Physiological and molecular responses of seedlings of an upland rice (‘Tung Lu 3’) to total submergence compared to those of a submergence-tolerant lowland rice (‘FR13A’). Rice 10, 42.CrossRefGoogle ScholarPubMed
Zheng, K, Subudhi, PK, Domingo, J, Magantay, G and Huang, N (1995) Rapid DNA isolation for marker assisted selection in rice breeding. Rice Genetics News Letter 12, 255–258.Google Scholar
Zhu, G, Chen, Y, Ella, ES and Ismail, AM (2018) Mechanisms associated with tiller suppression under stagnant flooding in rice. Journal of Agricultural Crop Science, 1–13.Google Scholar
Figure 0

Fig. 1. Phenotypic screening of RILs for anaerobic germination and SF.

Figure 1

Fig. 2. Frequency distribution of 184 RILs for plant survival % under anaerobic germination and SF.

Figure 2

Fig. 3. QTL for Anaerobic germination qAG 3.1on Chromosome 3.

Figure 3

Table 1. Summary of anaerobic germination and plant survival % under stagnant flooding among RILs

Figure 4

Table 2. Identified QTLs for flood tolerance using RILs of AC39416A

Figure 5

Fig. 4. QTL qSF10.1 for plant survival % under stagnant flooding.