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Identification of interspecific heterotic loci associated with agronomic traits in rice introgression lines carrying genomic fragments of Oryza glaberrima

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Abstract

In the present study, a set of 79 rice introgression lines (ILs) carrying variant introgressed segments of African rice (Oryza glaberrima Stued.) was used to identify quantitative trait loci (QTL) and heterotic loci (HL) associated with 7 agronomic traits. A total of 180 polymorphic markers between the donor and recurrent parents were found and 115 markers were used to identify the segregation of the introgression fragments. Based on the genotypic data of the ILs and test variety GZ63S as well as the phenotypic data of the IL and PIH, QTLs and HLs can be mapped on introgressed chromosome segments. One representative marker on each specific introgressed segment was defined as a QTL or a HL. 24 QTLs associated with six agronomic traits were mapped on 9 chromosomes and 23 interspecific HLs for seven agronomic traits were identified on 10 chromosomes in 2 years. Among them, 22 QTLs and 19 HLs were found to be associated with 5 yield-related traits respectively. The PIH (F1) testcross population showed superiority in most yield-related traits and was characterized by a high frequency of overdominant interspecific HLs. In addition, the pleiotropism was found in 5 marker loci for 11 QTLs associated with five agronomic traits and 4 marker loci for ten interspecific HLs for all the seven traits. This study is the first attempt for the identification of interspecific HLs between the two cultivated rice species, Asian rice (Oryza sativa L.) and African rice (O. glaberrima Steud.). Therefore, our results may help to lay the foundation for exploring the genetic mechanism of interspecific heterosis in rice.

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Abbreviations

DH:

Days to heading

FG:

Filled grain per panicle

GD:

Genetic diversity

GGT:

Graphical genotypes

GW:

Grains weight

HL:

Heterotic loci

IL:

Introgression line

LOD:

Logarithm of odds ratio

MPH:

Mid-parent heterosis

OD:

Over-dominance

PN:

Panicles per plant

PD:

Partial-dominance

PIH:

Partial interspecific hybrid

PH:

Plant height

P/TGMS:

Photo/thermo-sensitive genetic male sterility

PIC:

Polymorphism information content

QTL:

Quantitative trait loci

SN:

Spikelets per panicle

SS:

Seed setting rate

SSR:

Simple sequence repeats

References

  • Adedze YM, Efisue AA, Zhang SS, Samoura D, Huang F, He WC, Xie GS, Jin DM (2012) Identification of interspecific grain yield heterosis between two cultivated rice species Oryza sativa L. and Oryza glaberrima Steud. Austr J Crop Sci 6:1558–1564

    Google Scholar 

  • Agnoun Y, Sié M, Djedatin G, Dramé KN, Toulou B, Ogunbayo SA, Sanni KA, Tia D, Ahanchédé A, Vodouhè RS, Ndjiondjop MN (2012) Molecular profiling of interspecific lowland rice progenies resulting from crosses between TOG5681 and TOG5674 (Oryza glaberrima) and IR64 (Oryza sativa). Internat J Bio 4(3):19

    CAS  Google Scholar 

  • Aluko G, Martinez C, Tohme J, Castano C, Bergman C, Oard JH (2004) QTL mapping of grain quality traits from the interspecific cross Oryza sativa x O. glaberrima. Theor Appl Genet 109(3):630–639

    Article  CAS  PubMed  Google Scholar 

  • Biet E, Sun J, Dutreix M (1999) Conserved sequence preference in DNA binding among recombination proteins: an effect of ssDNA secondary structure. Nucleic Acids Res 27:596–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bimpong IK, Carpena AL, Mendioro MS, Fernandez JR, Ramos J, Reversat G, Brar DS (2010) Evaluation of Oryza sativa × Oryza glaberrima derived progenies for resistance to root knot nematode and identification of introgressed alien chromosome segments using SSR markers. Afr J Biotech 9:3988–3997

    CAS  Google Scholar 

  • Brandle JE, McVetty PBE (1990) Geographic diversity, parental selection, and heterosis in oilseed rape. Can J Plant Sci 70:935–940

    Article  Google Scholar 

  • Chen CJ, He WC, Nassirou TY, Zhou W, Yin YL, Dong XL, Rao QQ, Shi H, Zhao W, Efisue A, Jin DM (2016) Genetic diversity and phenotypic variation in an introgression line population derived from an interspecific cross between Oryza glaberrima and Oryza sativa. PLoS ONE 11(9):e0161746. doi:10.1371/journal.pone.0161746

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng SH, Li YC, Jie YZ et al (2007) Super hybrid rice breeding in China: achievements and prospects. J Integr Plant Biol 49(6):805–810

    Article  CAS  Google Scholar 

  • Dai XD, Ding YN, Tan LB, Fu YC, Liu FX, Zhu ZF, Sun XY, Sun XW, Gu P, Cai HW, Sun CQ (2012) HD1, an allele of DTH8/Ghd8, controls late heading date in common wild rice (Oryza rufipogon). J Integr Plant Biol 54:790–799

    Article  CAS  PubMed  Google Scholar 

  • Davenport CB (1908) Degeneration, albinism and inbreeding. Science 28(718):454–455

    Article  CAS  PubMed  Google Scholar 

  • Efisue AA, Tongoona P, Derera J, Ubi BE (2009) Screening early-generation progenies of interspecific rice genotypes for drought-stress tolerance during vegetative phase. J Crop Improv 23:174–193

    Article  CAS  Google Scholar 

  • Feng XM, Juan H, Qi HH, Huang YQ, Zhu LY, Zhao YF, Zheng Q, Li WZ, Bing Y (2012) Identification of heterotic loci for seven yield and yield-related traits in maize with a set of introgression lines. Austr J Crop Sci 6(12):1661–1665

    Google Scholar 

  • Fukuta Y, Konisho K, Senoo-Namai S, Yanagihara S, Tsunematsu H, Fukuo A, Kumashiro T (2012) Genetic characterization of rainfed upland New Rice for Afirca (NERICA) varieties. Breed Sci 62:27–37

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghesquière A, Séquier J, Second G, Lorieux M (1997) First steps towards a rational use of African rice, Oryza glaberrima, in rice breeding through a ‘contig line’ concept. Euphytica 96(1):31–39

    Article  Google Scholar 

  • Guo X, Guo YP, Ma J, Wang F, Sun MZ, Gui LJ, Zhou JJ, Song XL, Sun XZ, Zhang TZ (2013) Mapping heterotic loci for yield and agronomic traits using chromosome segment introgression lines in cotton. J Integr Plant Biol 55(8):759–774

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez AG, Carabali SJ, Giraldo OX, Martinez CP, Correa F, Prado G, Tohme J, Lorieux M (2010) Identification of a rice stripe necrosis virus resistance locus and yield component QTLs using Oryza sativa x O. glaberrima introgression lines. BMC Plant Bio. doi:10.1186/1471-2229-10-6

    Google Scholar 

  • Heuer S, Miezan KM (2003) Assessing hybrid sterility in Oryza glaberrima × O. sativa hybrid progenies by PCR marker analysis and crossing with wide compatibility varieties. Theor Appl Genet 107(5):902–909

    Article  CAS  PubMed  Google Scholar 

  • Hu FY, Tao DY, Yang YQ, Xu P, Li J, Zhou JW (2002) Studies of vegetative heterosis of interspecific hybrids between Oryza sativa and Oryza glaberrima. J Southwest Agric Univ 2002-02

  • Hu FY, Xu P, Deng XN et al (2006) Molecular mapping of a pollen killer gene S29 (t) in Oryza glaberrima and co-linear analysis with S22 in O. glumaepatula. Euphytica 151(3):273–278

    Article  CAS  Google Scholar 

  • Hu ZJ, He HH, Zhang SY, Sun F, Xin XY, Wang WX, Qian X, Yang JS, Luo XJ (2012) A kelch motif-containing serine/threonine protein phosphatase determines the large grain QTL trait in rice. J Integr Plant Biol 54:979–990

    Article  CAS  PubMed  Google Scholar 

  • Hua JP, Xing YZ, Wu WR, Xu CG, Sun XL, Yu SB, Zhang QF (2003) Single-locus heterotic effects and dominance by dominance interaction can adequately explain the genetic basis of heterosis in an elite hybrid. Proc Natl Acad Sci USA 100:2574–2579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang F, Xi F, Efisue AA, Zhang SS, Xie GS, He WC, Adedze YMN, Jin DM (2012) Genetically characterizing a new indica cytoplasmic male sterility with Oryza glaberrima cytoplasm for its potential use in hybrid rice production. Crop Sci 53(1):132–140. doi:10.2135/cropsci2012.07.0444

    Article  Google Scholar 

  • Hull FH (1945) Recurrent selection for specific combining ability in corn. J Am Soc Agron 37(2):134–145

    Article  Google Scholar 

  • Ikeda R, Yoshimi S, Inoussa A (2009) Seed fertility of F1 hybrids between upland rice NERICA cultivars and Oryza sativa L. or O.glaberrima Steud. Breed Sci 59:27–35

    Article  Google Scholar 

  • Ikehashi H, Araki H (1986) Genetics of F1 sterility in remote crosses of rice. Rice genetics. International Rice Research Institute, Manila, pp 119–130

    Google Scholar 

  • Jaikishan I, Rajendrakumar P, Ramesha MS et al (2010) Prediction of heterosis for grain yield in rice using key informative EST-SSR. Plant Breed 129(1):108–111

    Article  CAS  Google Scholar 

  • Jin DM, Nassirou TY (2015) Progress and perspectives of distant heterosis in rice. In: Al-Khayri JM, Jain SM, Dennis VJ (eds) Advances in plant breeding strategies: breeding, biotechnology and molecular tools, vol 1. Springer, Switzerland. doi:10.1007/978-3-319-22521-0

    Google Scholar 

  • Jin DM, Efisue AA, Zhang SS, et al. (2012) Developing a new indica CMS system and introgression restorer lines via interspecific crosses between Oryza glaberrima Steud. and Oryza sativa L. Abstract presented at the international conference on utilization of heterosis in crops, Xi’an, China, pp 264–265

  • Jones JW (1926) Hybrid vigour in rice. J Am Soc Agr 18(5):423–428

    Article  Google Scholar 

  • Jones MP, Dingkuhn M, DE Johnson, Sow A (1998) Growth and yield potential of Oryza sativa and O. glaberrima upland rice cultivars and their interspecific progenies. Field Crop Res 57(1):57–69

    Article  Google Scholar 

  • Li ZK, Xie QG, Zhu ZL, Liu JL, Han SX, Tian B, Yuan QQ, Tian JC (2010) Analysis of plant height heterosis based on QTL mapping in wheat. Acta Agron Sin 36:771–778

    CAS  Google Scholar 

  • Li F, Liu FH, Morinaga DZ (2011) A new gene for hybrid sterility from a cross between Oryza sativa and O. glaberrima. Plant Breed 130(2):165–171

    Article  CAS  Google Scholar 

  • Linares OF (2002) African rice (Oryza glaberrima): history and future potential. Proc Natl Acad Sci USA 99(25):16360–16365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu RH, Meng JL (2003) MapDraw: a Microsoft Excel macro for drawing genetic linkage maps based on given genetic linkage data. Heraditas (Beijing) 25(3):317–321

    Google Scholar 

  • Liu K, Muse SV (2005) PowerMaker: an integrated analysis environment for genetic maker analysis. Bioinformatics 21(9):2128–2129

    Article  CAS  PubMed  Google Scholar 

  • Lorieux M, Ndjiondjop MN, Ghesquière A (2000) A first interspecific Oryza sativa × Oryza glaberrima microsatellite-based genetic linkage map. Theor Appl Genet 100(3):593–601

    CAS  Google Scholar 

  • Luo XJ, Fu YC, Zhang PJ, Wu S, Tian F, Liu JY, Zhu ZF, Yang JS, Sun CQ (2009) Additive and over-dominant effects resulting from epistatic loci are the primary genetic basis of heterosis in rice. J Integr Plant Biol 51:393–408

    Article  PubMed  Google Scholar 

  • Luo XJ, Wu S, Tian F, Xin XY, Zha XJ, Dong XX, Fu YC, Wang XK, Yang JS, Sun CQ (2011) Identification of heterotic loci associated with yield-related traits in Chinese common wild rice (Oryza rufipogon Griff.). Plant Sci 181:14–22

    Article  CAS  PubMed  Google Scholar 

  • Ma LY, Bao JS, Guo LB, Zeng DL, Li XM, Ji ZJ, Xia YW, Yang CD, Qian Q (2009) Quantitative trait loci for panicle layer uniformity identified in doubled haploid lines of rice in two environments. J Integr Plant Biol 51:818–824

    Article  CAS  PubMed  Google Scholar 

  • Monforte AJ, Tanksley SD (2000) Development of a set of near isogenic and backcross recombinant inbred lines containing most of the Lycopersicon hirsutum genome in a L. esculentum genetic background: a tool for gene mapping and gene discovery. Genome 43:803–813

    Article  CAS  PubMed  Google Scholar 

  • Nassirou TY, He YQ (2011) NERICA: a hope for fighting hunger and poverty in Africa. Mol Plant Breed. doi:10.5376/mpb.2011.02.0011

    Google Scholar 

  • Ndjiondjop MN, Futakuchi K, Seck PA, Cisse F, Bocco R, Fatondji B (2012) Morpho-agronomic evaluation of Oryza glaberrima accessions and interspecific Oryza sativa × Oryza glaberrima derived lines under drought conditions. Afr J Agric Res 7:2527–2538

    Google Scholar 

  • Pasam RK, Sharma R, Malosetti M, van Eeuwijk FA et al (2012) Genome-wide association studies for agronomical traits in a worldwide spring barley collection. BMC Plant Biol 27:12–16

    Google Scholar 

  • Piffanelli P, Droc G, Mieulet D, Lanau N, Bes M, Bourgeois E, Rouviere C, Gavory F, Cruaud C, Ghesquière A et al (2007) Large-scale characterization of Tos17 insertion sites in a rice T-DNA mutant library. Plant Mol Biol 65(5):587–601

    Article  CAS  PubMed  Google Scholar 

  • Powers L (1944) An expansion of Jones’s theory for the explanation of heterosis. Am Nat 78:275–280

    Article  Google Scholar 

  • Qiu SQ, Liu K, Jiang JX et al (2005) Delimitation of the rice wide compatibility gene S5n to a 40-kb DNA fragment. Theor Appl Genet 111(6):1080–1086

    Article  CAS  PubMed  Google Scholar 

  • Sano Y (1986) Sterility barriers between Oryza sativa and O. glaberrima. International Rice Research Institute-Rice Genet, IRRI, Manila, pp 109–118

    Google Scholar 

  • Sarla N, Swamy B (2005) Oryza glaberrima a source for the improvement of Oryza sativa. Curr Sci 89(6):955–963

    Google Scholar 

  • Sasaki T (2003) Rice genome analysis: understanding the genetic secrets of the rice plant. Breed Sci 53(4):281–289

    Article  CAS  Google Scholar 

  • Semagn K, Ndjiondjop MN, Lorieux M, Cissoko M, Jones M, McCouch S (2007) Molecular profiling of an interspecific rice population derived from a cross between WAB 56-104 (Oryza sativa) and CG 14 (Oryza glaberrima). Afr J Biotech 6(17):2014–2022

    Article  CAS  Google Scholar 

  • Semel Y, Nissenbaum J, Menda N, Zinder M, Krieger U, Issman N, Pleban T, Lippman Z, Gur A, Zamir D (2006) Overdominant quantitative trait loci for yield and fitness in tomato. Proc Natl Acad Sci USA 103:12981–12986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen GJ, Zhan W, Chen HX, Xing YZ (2014) Dominance and epistasis are the main contributors to heterosis for plant height in rice. Plant Sci 215–216:11–18

    Article  PubMed  Google Scholar 

  • Syed NH, Chen ZJ (2005) Molecular marker genotypes, heterozygosity and genetic interactions explain heterosis in Arabidopsis thaliana. Heredity 94:295–304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang JH, Yan JB, Ma XQ, Teng WT, Wu WR, Dal JR, Dhillon BS, Mechinger AE, Li JS (2010) Dissection of the genetic basis of heterosis in an elite maize hybrid by QTL mapping in an immortalized F2 population. Theor Appl Genet 120:333–340

    Article  PubMed  Google Scholar 

  • Van Andel T (2010) African rice (Oryza glaberrima Steud.): lost crop of the enslaved Africans discovered in Suriname. Eco Bot 64(1):1–10

    Article  Google Scholar 

  • Van Berloo R (1999) GGT: software for the display of graphical genotypes. J Hered 90:328–329

    Article  Google Scholar 

  • Virmani SS, Chaudhary RC, Khush GS (1981) Current outlook on hybrid rice. Oryza 18:67–84

    Google Scholar 

  • Wang LQ, Zhao YF, Xue YD, Zhang ZX, Zheng YL, Chen JT (2007) Development and evaluation of two link-up single segment introgression lines (SSILs) in Zea mays. Acta Agron Sin 33:663–668

    CAS  Google Scholar 

  • Wang ZQ, Jian L, Yin CB, Wang XL, Lei JG, Xiao YL, Liu X, Liu SJ, Chen LM, Yu CY, Wan JM (2013) QTL mapping of heterotic loci of yield-related traits in rice. Chin J Rice Sci 27(6):569–576. doi:10.3969/j.issn1001G7216.2013.06.002

    Google Scholar 

  • Wang MH, Yu YS, Georg H, Pradeep RM et al (2014) The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication. Nature Genet. doi:10.1038/ng.3044

    Google Scholar 

  • Wang ZQ, Wang XL, Lei JG, Xiao YL, Li MZ, Yu CY (2015) QTL mapping and analysis of heterotic loci in three-line hybrid rice by using chromosome segment substitution lines. Acta Agric Univ Jiangxi 37(5):765–773. doi:10.13836/j.jjau.2015116

    CAS  Google Scholar 

  • Wang J, Li H, Zhang L, Meng L (2016) Users’ manual of QTL IciMapping. The Quantitative Genetics Group, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS), Genetic Resources Program, International Maize and Wheat Improvement Center (CIMMYT), Beijing, Mexico

    Google Scholar 

  • Wei XY, Bin W, Qian P, Feng W, Mao KJ, Zhang XG, Pei S, Liu ZH, Tang JH (2015) Heterotic loci for various morphological traits of maize detected using a single segment substitution lines test-cross population. Mol Breed 35:94. doi:10.1007/s11032-015-0287-4

    Article  Google Scholar 

  • Wing RA, Ammiraju JS, Luo M, Kim H, Yu Y, Kudrna D, Goicoechea JL, Wang W, Nelson W, Rao K et al (2005) The Oryza map alignment project: the golden path to unlocking the genetic potential of wild rice species. Plant Mol Biol 59(1):53–62

    Article  CAS  PubMed  Google Scholar 

  • Xin XY, Wang WX, Yang JS, Luo XJ (2011) Genetic analysis of heterotic loci detected in a cross between indica and japonica rice (Oryza sativa L.). Breed Sci 61:380–388

    Article  PubMed  PubMed Central  Google Scholar 

  • Young ND, Tanksley SD (1989) Restriction fragment length polymorphism maps and the concept of graphical genotypes. Theor Appl Genet 77:95–101

    Article  CAS  PubMed  Google Scholar 

  • Yu SB, Li JX, Xu CG, Tan YF, Gao YJ, Zhang QF, Maroof MA (1997) Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 94:9226–9231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao FM, Zhang GQ, Zeng RZ, Yang ZL, Ling YH, Sang XC, He GH (2011) Analysis of epistatic and additive effects of QTLs for grain shape using single segment substitution lines in rice (Oryza sativa L.). Acta Agron Sin 37:469–476

    Article  CAS  Google Scholar 

  • Zhuang JY, Fan YY, Wu JL, Xia YW, Zheng KL (2001) Overdominant effect plays an important role in heterosis of rice. Sci China Ser C 31:106–113

    Article  Google Scholar 

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Acknowledgements

We are thankful to Dr. Andrew A. Efisue, Ph.D., Departments of Crop and Soil Science, University of Port Harcourt, Port Harcourt, Nigeria, for providing the African rice variety material. This study was funded by the Fundamental Research Funds for the Central Universities (2013PY134), Specialized Research Fund for the Doctoral Program of Higher Education (20130146110026).

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Authors and Affiliations

  1. MOA Key Laboratory of Crop Ecophysiology and Farming System in the Middle Reaches of the Yangtze River, College of Plant Science and Technology, Huazhong Agricultural University, 430070, Wuhan, China

    Tondi Yacouba Nassirou, Wenchuang He, Caijin Chen, Athanase Nsabiyumva, Xilong Dong, Yilong Yin, Quanqin Rao, Wei Zhou, Han Shi, Wubin Zhao & Deming Jin

  2. State Key Laboratory of Rice Biology, China National Rice Research Institute, 310006, Hangzhou, China

    Adedze Y. M. Nevame

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  1. Tondi Yacouba Nassirou
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  2. Wenchuang He
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Correspondence to Deming Jin.

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Nassirou, T.Y., He, W., Chen, C. et al. Identification of interspecific heterotic loci associated with agronomic traits in rice introgression lines carrying genomic fragments of Oryza glaberrima . Euphytica 213, 176 (2017). https://doi.org/10.1007/s10681-017-1967-4

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