Improvement of grain yield under moisture and heat stress conditions through marker-assisted pedigree breeding in rice (Oryza sativa L.)
Darsha Manjula Withanawasam A , Madhavilatha Kommana A , Syamala Pulindala A , Aparna Eragam B , Vinodkumar N. Moode A , Amarnath Kolimigundla A , Ramanarao V. Puram C , Sudhakar Palagiri D , Ravindrareddy Balam E and Lakshminarayana R. Vemireddy A B *A Department of Genetics and Plant Breeding, S.V. Agricultural College, Acharya NG Ranga Agricultural University (ANGRAU), Tirupati-517502, Andhra Pradesh, India.
B Department of Molecular Biology and Biotechnology, S.V. Agricultural College, ANGRAU, Tirupati-517502, Andhra Pradesh, India.
C Regional Agricultural Research Station (RARS), ANGRAU, Maruteru, Andhra Pradesh, India.
D Regional Agricultural Research Station (RARS), ANGRAU, Tirupati, Andhra Pradesh, India.
E Department of Statistics and Computer Applications, S.V. Agricultural College, ANGRAU, Tirupati-517502, Andhra Pradesh, India.
Crop & Pasture Science 73(4) 356-369 https://doi.org/10.1071/CP21410
Submitted: 15 June 2021 Accepted: 17 November 2021 Published: 14 March 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Enhancement of rice (Oryza sativa L.) productivity under rainfed ecosystems is important to food security. Efforts to increase yield have had little success, mainly due to the complexity of inheritance of abiotic stress tolerance traits and the technical challenges of phenotyping these traits. The study was conducted to pyramid quantitative trait loci (QTLs) governing tolerance to moisture and heat stress from cv. Nagina22 and QTLs for high yield traits from variety IR64, with the aid of marker-assisted pedigree breeding. From the IR64/N22 cross, we identified 14 pyramided lines with various combinations of targeted QTLs (5–11 QTLs). The three best lines that performed well under moisture stress conditions were PL76 with two water-use efficiency (WUE) QTLs (Mr19a, SLA 9.1), three drought-tolerant yield (DTY) QTLs (qDTY1.2, qDTY3.2, qDTY6.1), one heat-tolerance (HT) QTL (qSSPF10) and four yield QTLs (qFLW4.1, qFLL9, LP1, GW5); PL476 with two WUE QTLs (%N11.1, qWue7a), two DTY QTLs (qDTY6.1, qDTY12.1), two HT QTLs (qSSPF10, qHT6) and three yield QTLs (qFLW4.1, qFLL9, LP1); and PL130 with two WUE QTLs (Mr19a, qWue7a), four DTY QTLs (qDTY1.2, qDTY3.2, qDTY4.1, qDTY12.1), two HT QTLs (qSSPF10, qHT6) and two yield QTLs (qFLW4.1, LP1). These three lines shown a yield advantage of 51.93%, 55.93% and 60.30%, respectively, over high-yielding IR64. Under heat stress, PL457 and PL130 with HT QTLs qSSPF10 and qHT6 showed 85.02% and 61.55% yield advantage, respectively, over IR64. In conclusion, we have demonstrated that the systematic combination of important QTLs from two contrasting parents through marker-assisted pedigree breeding is an outstanding approach to supplement conventional phenotype-based pedigree breeding, especially to improve complex traits such as yield and tolerance to moisture stress and heat.
Keywords: drought ressitance, grain yield, heat tolerance, marker assisted pedigree breeding, QTL pyramiding, pyramided lines, rice, water use efficiency.
References
Alma MH, Kalaycıoğlu H, Bektaş I, Tutus A (2005) Properties of cotton carpel-based particleboards. Industrial Crops and Products 22, 141–149.| Properties of cotton carpel-based particleboards.Crossref | GoogleScholarGoogle Scholar |
Anantha MS, Patel D, Quintana M, Swain P, Dwivedi JL, Torres RO, Verulkar SB, Variar M, Mandal NP, Kumar A, Henry A (2016) Trait combinations that improve rice yield under drought: Sahbhagi Dhan and new drought-tolerant varieties in South Asia. Crop Science 56, 408–421.
| Trait combinations that improve rice yield under drought: Sahbhagi Dhan and new drought-tolerant varieties in South Asia.Crossref | GoogleScholarGoogle Scholar |
Anyaoha CO, Fofana M, Gracen V, Tongoona P, Mande S (2019) Introgression of two drought QTLs into FUNAABOR-2 early generation backcross progenies under drought stress at reproductive stage. Rice Science 26, 32–41..
| Introgression of two drought QTLs into FUNAABOR-2 early generation backcross progenies under drought stress at reproductive stage.Crossref | GoogleScholarGoogle Scholar |
Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309, 741–745.
| Cytokinin oxidase regulates rice grain production.Crossref | GoogleScholarGoogle Scholar | 15976269PubMed |
Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW (1992) A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environmental and Experimental Botany 32, 85–100.
| A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants.Crossref | GoogleScholarGoogle Scholar |
Barrs HD, Weatherlay PE (1962) A reexamination of the relative turgidity techniques for estimating water deficit in leaves. Australian Journal of Biological Sciences 15, 413–428.
| A reexamination of the relative turgidity techniques for estimating water deficit in leaves.Crossref | GoogleScholarGoogle Scholar |
Bernier J, Kumar A, Ramaiah V, Spaner D, Atlin GN (2007) A large-effect QTL for grain yield under reproductive-stage drought stress in upland rice. Crop Science 47, 507–516.
| A large-effect QTL for grain yield under reproductive-stage drought stress in upland rice.Crossref | GoogleScholarGoogle Scholar |
Bharathkumar S, Pragnya PJ, Jitendra K, Archana B, Singh ON, Reddy JN (2014) Identification of rice germplasms associated with microsatelite (SSR) markers for heat tolerance at reproductive stage and expression of heat stress related gene. Indian Research Journel of Genetics and Biotechnologyy 6, 424–427.
Bhukya JN, Bollineni SN, Kadambari G, Bommisetty R, Gudikati ER, Withanawasam DM, Issa K, Akkareddy S, Eslavath SN, Dokuparthi AK, Ergam A, Moode VN, Pottepalem R, Chintala S, Narrareddy EP, Tanti B, Nimai MP, Muniraju P, Janaki YV, Vermireddy LR (2020) Marker-assisted introgression of QTLs foryield under moisture stress into elite varieties of rice (Oryza sativa L.). Plant Breeding 139, 1076–1089.
| Marker-assisted introgression of QTLs foryield under moisture stress into elite varieties of rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
Casartelli A, Riewe D, Hubberten HM, Altmann T, Hoefgen R, Heuer S (2018) Exploring traditional aus-type rice for metabolites conferring drought tolerance. Rice 11, 9
| Exploring traditional aus-type rice for metabolites conferring drought tolerance.Crossref | GoogleScholarGoogle Scholar | 29372429PubMed |
Cheng LR, Wang JM, Uzokwe V, Meng LJ, Wang Y, Sun Y, Zhu LH, Xu JL, Li ZK (2012) Genetic analysis of cold tolerance at seedling stage and heat tolerance at anthesis in rice (Oryza sativa L.). Journal of Integrative Agriculture 11, 359–367.
| Genetic analysis of cold tolerance at seedling stage and heat tolerance at anthesis in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
Dixit S, Yadaw RB, Mishra KK, Kumar A (2017) Marker-assisted breeding to develop the drought-tolerant version of Sabitri, a popular variety from Nepal. Euphytica 213, 184
| Marker-assisted breeding to develop the drought-tolerant version of Sabitri, a popular variety from Nepal.Crossref | GoogleScholarGoogle Scholar | 33364630PubMed |
Fu X, Xu J, Zhou M, Chen M, Shen L, Li T, Zhu Y, Wang J, Hu J, Zhu L, Gao Z, Dong G, Guo L, Ren D, Chen G, Lin J, Qian Q, Zhang G (2019) Enhanced expression of QTL qLL9/DEP1 facilitates the improvement of leaf morphology and grain yield in rice. International Journal of Molecular Sciences 20, 866
| Enhanced expression of QTL qLL9/DEP1 facilitates the improvement of leaf morphology and grain yield in rice.Crossref | GoogleScholarGoogle Scholar |
Ghimire KH, Quiatchon LA, Vikram P, Swamy BPM, Dixit S, Ahmed H, Hernandez JE, Borromeo TH, Kumar A (2012) Identification and mapping of a QTL (qDTY1.1) with a consistent effect on grain yield under drought. Field Crops Research 131, 88–96.
| Identification and mapping of a QTL (qDTY1.1) with a consistent effect on grain yield under drought.Crossref | GoogleScholarGoogle Scholar |
Gosal SS, Wani SH, Kang MS (2009) Biotechnology and drought tolerance. Journal of Crop Improvement 23, 19–54.
| Biotechnology and drought tolerance.Crossref | GoogleScholarGoogle Scholar |
Huang X, Qian Q, Liu Z, Sun H, He S, Luo D, Xia G, Chu C, Li J, Fu X (2009) Natural variation at the DEP1 locus enhances grain yield in rice. Nature Genetics 41, 494–497.
| Natural variation at the DEP1 locus enhances grain yield in rice.Crossref | GoogleScholarGoogle Scholar | 19305410PubMed |
Hu SP, Mei HW, Liu HY, Zou GH, Liu GL, Yu XQ, Li J, Long P, Luo L (2004) Molecular dissection on rice photosynthesis-related traitsat reproductive stage in irrigated and drought conditions. In ‘Resilient crops for water limited environments. Proceedings of a workshop held at Cuernavaca, Mexico, 24–28 May 2004’. (Eds D Poland, M Sawkins, J-M Ribaut, D Hoisington) pp. 43–44. (CIMMYT: Mexico City, Mexico)
Kumar A, Dixit S, Ram T, Yadaw RB, Mishra KK, Mandal NP (2014) Breeding high-yielding drought-tolerant rice: genetic variations and conventional and molecular approaches. Journal of Experimental Botany 65, 6265–6278.
| Breeding high-yielding drought-tolerant rice: genetic variations and conventional and molecular approaches.Crossref | GoogleScholarGoogle Scholar | 25205576PubMed |
Kumar A, Sandhu N, Venkateshwarlu C, Priyadarshi R, Yadav S, Majumder RR, Singh VK (2020) Development of introgression lines in high yielding, semi-dwarf genetic backgrounds to enable improvement of modern rice varieties for tolerance to multiple abiotic stresses free from undesirable linkage drag. Scientific Reports 10, 13073
| Development of introgression lines in high yielding, semi-dwarf genetic backgrounds to enable improvement of modern rice varieties for tolerance to multiple abiotic stresses free from undesirable linkage drag.Crossref | GoogleScholarGoogle Scholar | 32753648PubMed |
Lang NT, Ha PTT, Tru PC, Toan TB, Buu BC, Cho YC (2015) Breeding for heat tolerance rice based on marker-assisted backcrosing in Vietnam. Plant Breeding and Biotechnology 3, 274–281.
| Breeding for heat tolerance rice based on marker-assisted backcrosing in Vietnam.Crossref | GoogleScholarGoogle Scholar |
Liu E, Liu Y, Wu G, Zeng S, Tran Thi TG, Liang L, Liang Y, Dong Z, She D, Wang H, Zaid IU, Hong D (2016) Identification of a candidate gene for panicle length in rice (Oryza sativa L.) via association and linkage analysis. Frontiers in Plant Science 7, 596
| Identification of a candidate gene for panicle length in rice (Oryza sativa L.) via association and linkage analysis.Crossref | GoogleScholarGoogle Scholar | 27200064PubMed |
Liu Q, Yang T, Yu T, Zhang S, Mao X, Zhao J, Wang X, Dong J, Liu B (2017) Integrating small RNA sequencing with QTL mapping for identification of miRNAs and their target genes associated with heat tolerance at the flowering stage in rice. Frontiers in Plant Science 8, 43
| Integrating small RNA sequencing with QTL mapping for identification of miRNAs and their target genes associated with heat tolerance at the flowering stage in rice.Crossref | GoogleScholarGoogle Scholar | 28174587PubMed |
Mackill DJ, Khush GS (2018) IR64: a high-quality and high-yielding mega variety. Rice 11, 18
| IR64: a high-quality and high-yielding mega variety.Crossref | GoogleScholarGoogle Scholar | 29629479PubMed |
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8, 4321–4326.
| Rapid isolation of high molecular weight plant DNA.Crossref | GoogleScholarGoogle Scholar | 7433111PubMed |
Muthu V, Abbai R, Nallathambi J, Rahman H, Ramasamy S, Kambale R, Thulasinathan T, Ayyenar B, Muthurajan R (2020) Pyramiding QTLs controlling tolerance against drought, salinity, and submergence in rice through marker assisted breeding. PLoS ONE 15, e0227421
| Pyramiding QTLs controlling tolerance against drought, salinity, and submergence in rice through marker assisted breeding.Crossref | GoogleScholarGoogle Scholar | 31910435PubMed |
Qu Y, Mu P, Zhang H, Chen CY, Gao Y, Tian Y, Wen F, Li Z (2008) Mapping QTLs of root morphological traits at different growth stages in rice. Genetica 133, 187–200.
| Mapping QTLs of root morphological traits at different growth stages in rice.Crossref | GoogleScholarGoogle Scholar | 17823843PubMed |
Sandhu N, Kumar A (2017) Bridging the rice yield gaps under drought: QTLs, genes, and their use in breeding programs. Agronomy 7, 27
| Bridging the rice yield gaps under drought: QTLs, genes, and their use in breeding programs.Crossref | GoogleScholarGoogle Scholar |
Shamsudin NAA, Swamy BPM, Ratnam W, Cruz MTS, Raman A, Kumar A (2016) Marker assisted pyramiding of drought yield QTLs into a popular Malaysian rice cultivar, MR219. BMC Genetics 17, 30
| Marker assisted pyramiding of drought yield QTLs into a popular Malaysian rice cultivar, MR219.Crossref | GoogleScholarGoogle Scholar |
Shankar R, Bhattacharjee A, Jain M (2016) Transcriptome analysis in different rice cultivars provides novel insights into desiccation and salinity stress responses. Scientific Reports 6, 23719
| Transcriptome analysis in different rice cultivars provides novel insights into desiccation and salinity stress responses.Crossref | GoogleScholarGoogle Scholar | 27029818PubMed |
Srinivasan S, Gomez SM, Kumar SS, Ganesh SK, Biji KR, Senthil A, Babu RC (2008) QTLs linked to leaf epicuticular wax, physio-morphological and plant production traits under drought stress in rice (Oryza sativa L.). Plant Growth Regulation 56, 245–256.
| QTLs linked to leaf epicuticular wax, physio-morphological and plant production traits under drought stress in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
Sudhakar P, Latha P, Reddy PV (2016) In ‘Phenotyping crop plants for physiological and biochemical traits’. pp. 53–64. (BSP Books: Hyderabad, India)
Swamy BPM, Ahmed HU, Henry A, Mauleon R, Dixit S, Vikram P, Tilatto R, Verulkar SB, Perraju P, Mandal NP, Variar M, Robin S, Chandrababu R, Singh ON, Dwivedi JL, Das SP, Mishra KK, Yadaw RB, Aditya TL, Karmakar B, Satoh K, Moumeni A, Kikuchi S, Leung H, Kumar A (2013) Genetic, physiological, and gene expression analyses reveal that multiple QTL enhance yield of rice mega variety IR64 under drought. PLoS ONE 8, e62795
| Genetic, physiological, and gene expression analyses reveal that multiple QTL enhance yield of rice mega variety IR64 under drought.Crossref | GoogleScholarGoogle Scholar |
Tabkhkar N, Rabiei B, Samizadeh Lahiji H, Hosseini Chaleshtori M (2018) Genetic variation and association analysis of the SSR markers linked to the major drought–yield QTLs of rice. Biochemical Genetics 56, 356–374.
| Genetic variation and association analysis of the SSR markers linked to the major drought–yield QTLs of rice.Crossref | GoogleScholarGoogle Scholar | 29478138PubMed |
Tagle AG, Fujita D, Ebron LA, Telebanco-Yanoria MJ, Sasaki K, Ishimaru T, Fukuta Y, Kobayashi N (2016) Characterization of QTL for unique agronomic traits of new-plant-type rice varieties using introgression lines of IR64. The Crop Journal 4, 12–20.
| Characterization of QTL for unique agronomic traits of new-plant-type rice varieties using introgression lines of IR64.Crossref | GoogleScholarGoogle Scholar |
This D, Comstock J, Courtois B, Xu Y, Ahmadi N, Vonhof WM, Fleet C, Setter T, McCouch S (2010) Genetic analysis of water use efficiency in rice (Oryza sativa L.) at the leaf level. Rice 3, 72–86.
| Genetic analysis of water use efficiency in rice (Oryza sativa L.) at the leaf level.Crossref | GoogleScholarGoogle Scholar |
Venuprasad R, Lafitte HR, Atlin GN (2007) Response to direct selection for grain yield under drought stress in rice. Crop Science 47, 285–293.
| Response to direct selection for grain yield under drought stress in rice.Crossref | GoogleScholarGoogle Scholar |
Venuprasad R, Dalid CO, Del Valle M, Zhao D, Espiritu M, Sta Cruz MT, Amante M, Kumar A, Atlin GN (2009) Identification and characterization of large-effect quantitative trait loci for grain yield under lowland drought stress in rice using bulk-segregant analysis. Theoretical and Applied Genetics 120, 177–190.
| Identification and characterization of large-effect quantitative trait loci for grain yield under lowland drought stress in rice using bulk-segregant analysis.Crossref | GoogleScholarGoogle Scholar | 19841886PubMed |
Venuprasad R, Bool ME, Quiatchon L, Atlin GN (2012) A QTL for rice grain yield in aerobic environments with large effects in three genetic backgrounds. Theoretical and Applied Genetics 124, 323–332.
| A QTL for rice grain yield in aerobic environments with large effects in three genetic backgrounds.Crossref | GoogleScholarGoogle Scholar | 21938473PubMed |
Vikram P, Swamy BPM, Dixit S, Ahmed HU, Cruz MTS, Singh AK, Kumar A (2011) qDTY1.1, a major QTL for rice grain yield under reproductive-stage drought stress with a consistent effect in multiple elite genetic backgrounds. BMC Genetics 12, 89
| qDTY1.1, a major QTL for rice grain yield under reproductive-stage drought stress with a consistent effect in multiple elite genetic backgrounds.Crossref | GoogleScholarGoogle Scholar | 22008150PubMed |
Vikram P, Swamy BPM, Dixit S, Trinidad J, Cruz MTS, Maturan PC, Amante M, Kumar A (2016) Linkages and interactions analysis of major effect drought grain yield QTLs in rice. PLoS ONE 11, e0151532
| Linkages and interactions analysis of major effect drought grain yield QTLs in rice.Crossref | GoogleScholarGoogle Scholar | 27018583PubMed |
Weng J, Gu S, Wan X, Gao H, Guo T, Su N, Lei C, Zhang X, Cheng Z, Guo X, Wang J, Jiang L, Zhai H, Wan J (2008) Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Research 18, 1199–1209.
| Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight.Crossref | GoogleScholarGoogle Scholar | 19015668PubMed |
Xiao Y, Pan Y, Luo L, Zhang G, Deng H, Dai L, Liu X, Tang W, Chen L, Wang G-L (2011) Quantitative trait loci associated with seed set under high temperature stress at the flowering stage in rice (Oryza sativa L.). Euphytica 178, 331–338.
| Quantitative trait loci associated with seed set under high temperature stress at the flowering stage in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
Xie X, Song M-H, Jin F, Ahn S-N, Suh J-P, Hwang H-G, McCouch SR (2006) Fine mapping of a grain weight quantitative trait locus on rice chromosome 8 using near-isogenic lines derived from a cross between Oryza sativa and Oryza rufipogon. Theoretical and Applied Genetics 113, 885–894.
| Fine mapping of a grain weight quantitative trait locus on rice chromosome 8 using near-isogenic lines derived from a cross between Oryza sativa and Oryza rufipogon.Crossref | GoogleScholarGoogle Scholar | 16850315PubMed |
Ye C, Tenorio FA, Argayoso MA, Laza MA, Koh H-J, Redoña ED, Jagadish KSV, Gregorio GB (2015) Identifying and confirming quantitative trait loci associated with heat tolerance at flowering stage in different rice populations. BMC Genetics 16, 41
| Identifying and confirming quantitative trait loci associated with heat tolerance at flowering stage in different rice populations.Crossref | GoogleScholarGoogle Scholar | 25895682PubMed |
Zafar SA, Hameed A, Nawaz MA, Wei MA, Noor MA, Hussain M, Rahman M (2018) Mechanisms and molecular approaches for heat tolerance in rice (Oryza sativa L.) under climate change scenario. Journal of Integrative Agriculture 17, 726–738.
| Mechanisms and molecular approaches for heat tolerance in rice (Oryza sativa L.) under climate change scenario.Crossref | GoogleScholarGoogle Scholar |
Zu X, Lu Y, Wang Q, Chu P, Miao W, Wang H, La H (2017) A new method for evaluating the drought tolerance of upland rice cultivars. The Crop Journal 5, 488–498.
| A new method for evaluating the drought tolerance of upland rice cultivars.Crossref | GoogleScholarGoogle Scholar |