Advertisement

Euphytica

, 215:153 | Cite as

Using genome conservation between Lotus japonicus and agronomically important Lotus species for discovering drought tolerance QTLs

  • Luis InostrozaEmail author
  • Hernán Acuña
  • José Méndez
  • Mehul Bhakta
  • Salvador A. Gezan
Article
  • 27 Downloads

Abstract

Lotus tenuis is a perennial forage legume species closely related to the model legume L. japonicus. Genetic relatedness between cultivated and model Lotus species has not been exploited so far. Furthermore, L. tenuis drought tolerance cultivars for marginal environments are in high demand. Marker-assisted selection is a modern breeding tool that allows to dissect genetically complex traits such as drought tolerance and to select for favorable alleles. However, L. tenuis is considered an orphan crop because no genome sequencing effort has been made. The objective of this work was to perform association mapping analyses on a L. tenuis population (LtAM) comprised of 100 genotypes for identifying genomic regions (QTLs) controlling drought tolerance. The LtAM population was established on a two-water regime (rainfed and irrigated) under a Mediterranean climate condition. Phenotyping was carried out during two growing seasons and included the measurement of important physiological and agronomical traits. Genetic characterization was performed with 88 transferable simple sequence repeats (SSR) molecular markers from L. japonicus genome. Association mapping analyses allowed to identify 40 marker-trait associations, almost 50% of them were found on chromosomes two and six of L. japonicus genome. For seven SSR-markers, 11 putative candidate genes were found. Based on annotations from the Medicago truncatula and Arabidopsis thaliana genomes, these genes could plausibly be candidates of causative polymorphism altering biochemical and physiological functions involved in the abiotic stress responses.

Keywords

Forage legumes Physiological traits Simple sequence repeats Marker assisted selection 

Notes

Acknowledgements

This work was funded by FONDECYT 11100094 and MINAGRI-INIA-501364–70 research projects.

Supplementary material

10681_2019_2475_MOESM1_ESM.xlsx (20 kb)
Supplementary file1 (XLSX 20 kb)

References

  1. Acuña H, Hellman P, Barrientos L, Figueroa M, Fuente Adl (2004) Estimación de la fijación de nitrógeno en tres especies del genero Lotus por el método de la dilución isotópica. Agro-Ciencia 20(1):5–15Google Scholar
  2. Acuña H, Concha A, Figueroa M (2008) Condensed tannin concentrations of three Lotus species grown in different environments. Chil J Agric Res 68(1):31–41CrossRefGoogle Scholar
  3. Acuña H, Inostroza L, Paulina Sanchez M, Tapia G (2010a) Drought-tolerant naturalized populations of Lotus tenuis for constrained environments. Acta Agric Scand Sect B-Soil Plant Sci 60(2):174–181.  https://doi.org/10.1080/09064710902800224 CrossRefGoogle Scholar
  4. Acuña H, Inostroza L, Sánchez MP, Tapia G (2010b) Drought-tolerant naturalized populations of Lotus tenuis for constrained environments. Acta Agric Scand Sect B-Soil Plant Sci 60(2):174–181.  https://doi.org/10.1080/09064710902800224 CrossRefGoogle Scholar
  5. Afzal AJ, Wood AJ, Lightfoot DA (2008) Plant receptor-like serine threonine kinases: roles in signaling and plant defense. Mol Plant-microbe Interactions MPMI 21(5):507–517.  https://doi.org/10.1094/mpmi-21-5-0507 CrossRefGoogle Scholar
  6. Alves MS, Fontes EPB, Fietto LG (2011) EARLY RESPONSIVE to DEHYDRATION 15, a new transcription factor that integrates stress signaling pathways. Plant Signaling Behavior 6(12):1993–1996.  https://doi.org/10.4161/psb.6.12.18268 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Barrett BA, Faville MJ, Nichols SN, Simpson WR, Bryan GT, Conner AJ (2015) Breaking through the feed barrier: options for improving forage genetics. Animal Production Science 55(7):883–892.  https://doi.org/10.1071/AN14833 CrossRefGoogle Scholar
  8. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635.  https://doi.org/10.1093/bioinformatics/btm308 CrossRefPubMedGoogle Scholar
  9. Bradshaw JE (2017) Plant breeding: past, present and future. Euphytica 213(3):60.  https://doi.org/10.1007/s10681-016-1815-y CrossRefGoogle Scholar
  10. Butler DG, Cullis BR, Gilmour AR, Gogel BJ (2009) Mixed models for S language environments: ASReml-R reference manual. Queensland Department of Primary Industries, Brisbane, AustraliaGoogle Scholar
  11. Choi H-K, Mun J-H, Kim D-J, Zhu H, Baek J-M, Mudge J, Roe B, Ellis N, Doyle J, Kiss GB, Young ND, Cook DR (2004) Estimating genome conservation between crop and model legume species. Proc Natl Acad Sci USA 101(43):15289–15294.  https://doi.org/10.1073/pnas.0402251101 CrossRefGoogle Scholar
  12. Cobb JN, DeClerck G, Greenberg A, Clark R, McCouch S (2013) Next-generation phenotyping: requirements and strategies for enhancing our understanding of genotype–phenotype relationships and its relevance to crop improvement. Theor Appl Genet 126(4):867–887.  https://doi.org/10.1007/s00122-013-2066-0 CrossRefPubMedGoogle Scholar
  13. Dobrowolski M, Forster JW (2007) Linkage disequilibrium-based association mapping in forage species. In: Oraguzie NC, Rikkerink EHA, Gardiner SE, Silva HND (eds) Association mapping in plants. Springer, New York, pp 197–210CrossRefGoogle Scholar
  14. Ekué MRM, Gailing O, Finkeldey R (2009) Transferability of simple sequence repeat (SSR) markers developed in litchi chinensis to blighia sapida (Sapindaceae). Plant Mol Biol Rep 27(4):570–574.  https://doi.org/10.1007/s11105-009-0115-2 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14(8):2611–2620.  https://doi.org/10.1111/j.1365-294X.2005.02553.x CrossRefPubMedGoogle Scholar
  16. Gondo T, Sato S, Okumura K, Tabata S, Akashi R, Isobe S (2007) Quantitative trait locus analysis of multiple agronomic traits in the model legume Lotus japonicus. Genome 50(7):627–637.  https://doi.org/10.1139/g07-040 CrossRefPubMedGoogle Scholar
  17. Grant W (2004) List of Lotus corniculatus (Birdsfoot trefoil), L. uliginosus/ L. pedunculatus (Big trefoil), L. glaber (Narrowleaf trefoil) and L. subbiflorus cultivars. Part 1. Cultivars with known or tentative country of origin. Lotus Newslett 34:12–26Google Scholar
  18. Hayashi M, Miyahara A, Sato S, Kato T, Yoshikawa M, Taketa M, Hayashi M, Pedrosa A, Onda R, Imaizumi-Anraku H, Bachmair A, Sanda N, Stougaard J, Murooka Y, Tabata S, Kawasaki S, Kawaguchi M, Harada K (2001) Construction of a genetic linkage map of the model legume Lotus japonicus using an intraspecific F 2 population. DNA Res 8(6):301–310.  https://doi.org/10.1093/dnares/8.6.301 CrossRefPubMedGoogle Scholar
  19. Hirsch S, Oldroyd GED (2009) GRAS-domain transcription factors that regulate plant development. Plant Signal Behav 4(8):698–700CrossRefGoogle Scholar
  20. Inostroza L, Acuña H, Méndez J (2015a) Multi-physiological-trait selection indices to identify Lotus tenuis genotypes with high dry matter production under drought conditions. Crop Pasture Sci 66(1):90–99.  https://doi.org/10.1071/CP14193 CrossRefGoogle Scholar
  21. Inostroza L, Acuna H, Tapia G (2015b) Relationships between phenotypic variation in osmotic adjustment, water-use efficiency, and drought tolerance of seven cultivars of Lotus corniculatus L. Chil J Agric Res 75(1):3–12.  https://doi.org/10.4067/s0718-58392015000100001 CrossRefGoogle Scholar
  22. Inostroza L, Acuna H, Munoz P, Vasquez C, Ibanez J, Tapia G, Pino MT, Aguilera H (2016) Using aerial images and canopy spectral reflectance for high-throughput phenotyping of white clover. Crop Sci 56(5):2629–2637.  https://doi.org/10.2135/cropsci2016.03.0156 CrossRefGoogle Scholar
  23. Kaur S, Francki MG, Forster JW (2012) Identification, characterization and interpretation of single-nucleotide sequence variation in allopolyploid crop species. Plant Biotechnol J 10(2):125–138.  https://doi.org/10.1111/j.1467-7652.2011.00644.x CrossRefGoogle Scholar
  24. Klein MA, Grusak MA (2009) Identification of nutrient and physical seed trait QTL in the model legume Lotus japonicus. Genome 52(8):677–691.  https://doi.org/10.1139/g09-039 CrossRefPubMedGoogle Scholar
  25. Klein MA, Lopez-Millan AF, Grusak MA (2012) Quantitative trait locus analysis of root ferric reductase activity and leaf chlorosis in the model legume. Lotus Japonicus Plant Soil 351(1–2):363–376.  https://doi.org/10.1007/s11104-011-0972-y CrossRefGoogle Scholar
  26. Kramina TE, Degtjareva GV, Samigullin TH, Valiejo-Roman CM, Kirkbride JH, Volis S, Deng T, Sokoloff DD (2016) Phylogeny of Lotus (Leguminosae: Loteae): Partial incongruence between nrITS, nrETS and plastid markers and biogeographic implications. Taxon 65(5):997–1018.  https://doi.org/10.12705/655.4 CrossRefGoogle Scholar
  27. Licausi F, Ohme-Takagi M, Perata P (2013) APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199(3):639–649.  https://doi.org/10.1111/nph.12291 CrossRefGoogle Scholar
  28. Mackay TFC (2001) The genetic architecture of quantitative traits. Ann Rev Genet 35(1):303–339.  https://doi.org/10.1146/annurev.genet.35.102401.090633 CrossRefPubMedGoogle Scholar
  29. Manzur ME, Grimoldi AA, Insausti P, Striker GG (2009) Escape from water or remain quiescent? Lotus tenuis changes its strategy depending on depth of submergence. Ann Bot 104(6):1163–1169.  https://doi.org/10.1093/aob/mcp203 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Mauri N, Fernández-Marcos M, Costas C, Desvoyes B, Pichel A, Caro E, Gutierrez C (2016) GEM, a member of the GRAM domain family of proteins, is part of the ABA signaling pathway. Sci Rep 6:22660.  https://doi.org/10.1038/srep22660 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Niels S, Jin HJ, Dulce NRN, Francisco T, Cristina C, Andreas B, Shusei S, Masayoshi K, Satoshi T, Parnliske M, Jose ERS, Stig UA, Jens S (2012) A set of Lotus japonicus Gifu x Lotus burttii recombinant inbred lines facilitates map-based cloning and QTL mapping. DNA Res 19(4):317–323.  https://doi.org/10.1093/dnares/dss014 CrossRefGoogle Scholar
  32. Parsons AJ, Edwards GR, Newton PCD, Chapman DF, Caradus JR, Rasmussen S, Rowarth JS (2011) Past lessons and future prospects: plant breeding for yield and persistence in cool-temperate pastures. Grass Forage Sci 66(2):153–172.  https://doi.org/10.1111/j.1365-2494.2011.00785.x CrossRefGoogle Scholar
  33. Peakall R, Gilmore S, Keys W, Morgante M, Rafalski A (1998) Cross-species amplification of soybean (Glycine max) simple sequence repeats (SSRs) within the genus and other legume genera: implications for the transferability of SSRs in plants. Mol Biol Evol 15(10):1275–1287.  https://doi.org/10.1093/oxfordjournals.molbev.a025856 CrossRefGoogle Scholar
  34. Pirnajmedin F, Majidi MM, Saeidi G, Gheysari M, Nourbakhsh V, Radan Z (2017) Genetic analysis of root and physiological traits of tall fescue in association with drought stress conditions. Euphytica 213(7):135.  https://doi.org/10.1007/s10681-017-1920-6 CrossRefGoogle Scholar
  35. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959PubMedPubMedCentralGoogle Scholar
  36. Quirino BF, Reiter W-D, Amasino RD (2001) One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated. Plant Mol Biol 46(4):447–457.  https://doi.org/10.1023/a:1010639015959 CrossRefPubMedGoogle Scholar
  37. Ranocha P, Denancé N, Vanholme R, Freydier A, Martinez Y, Hoffmann L, Köhler L, Pouzet C, Renou J-P, Sundberg B, Boerjan W, Goffner D (2010) Walls are thin 1 (WAT1), an Arabidopsis homolog of Medicago truncatula NODULIN21, is a tonoplast-localized protein required for secondary wall formation in fibers. Plant J 63(3):469–483.  https://doi.org/10.1111/j.1365-313X.2010.04256.x CrossRefPubMedGoogle Scholar
  38. Real D, Warden J, Sandral GA, Colmer TD (2008) Waterlogging tolerance and recovery of 10 Lotus species. Aust J Exp Agric 48(4):480–487.  https://doi.org/10.1071/ea07110 CrossRefGoogle Scholar
  39. Robins JG, Bauchan GR, Brummer EC (2007) Genetic mapping forage yield, plant height, and regrowth at multiple harvests in tetraploid alfalfa (Medicago sativa L). Crop Sci 47(1):11–18.  https://doi.org/10.2135/cropsci2006.07.0447 CrossRefGoogle Scholar
  40. Saha MC, Cooper JD, Mian MAR, Chekhovskiy K, May GD (2006) Tall fescue genomic SSR markers: development and transferability across multiple grass species. Theor Appl Genet 113(8):1449–1458.  https://doi.org/10.1007/s00122-006-0391-2 CrossRefPubMedGoogle Scholar
  41. Sakiroglu M, Brummer EC (2016) Identification of loci controlling forage yield and nutritive value in diploid alfalfa using GBS-GWAS. Theor Appl Genet 130:1–8.  https://doi.org/10.1007/s00122-016-2782-3 CrossRefGoogle Scholar
  42. Sato S, Tabata S (2006) Lotus japonicus as a platform for legume research. Curr Opin Plant Biol 9(2):128–132.  https://doi.org/10.1016/j.pbi.2006.01.008 CrossRefGoogle Scholar
  43. Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T, Nakao M, Sasamoto S, Watanabe A, Ono A, Kawashima K, Fujishiro T, Katoh M, Kohara M, Kishida Y, Minami C, Nakayama S, Nakazaki N, Shimizu Y, Shinpo S, Takahashi C, Wada T, Yamada M, Ohmido N, Hayashi M, Fukui K, Baba T, Nakamichi T, Mori H, Tabata S (2008) Genome structure of the legume. Lotus Japonicus DNA Res 15(4):227–239.  https://doi.org/10.1093/dnares/dsn008 CrossRefPubMedGoogle Scholar
  44. Shah N, Hirakawa H, Kusakabe S, Sandal N, Stougaard J, Schierup MH, Sato S, Andersen SU (2016) High-resolution genetic maps of Lotus japonicus and L-burttii based on re-sequencing of recombinant inbred lines. DNA Res 23(5):487–494.  https://doi.org/10.1093/dnares/dsw033 CrossRefPubMedCentralGoogle Scholar
  45. Shirasawa K, Isobe S, Tabata S, Hirakawa H (2014) Kazusa Marker DataBase: a database for genomics, genetics, and molecular breeding in plants. Breed Sci 64(3):264–271.  https://doi.org/10.1270/jsbbs.64.264 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Skubacz A, Daszkowska-Golec A, Szarejko I (2016) The role and regulation of ABI5 (ABA-Insensitive 5) in plant development, abiotic stress responses and phytohormone crosstalk. Front Plant Sci 7:1884.  https://doi.org/10.3389/fpls.2016.01884 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci 100(16):9440–9445.  https://doi.org/10.1073/pnas.1530509100 CrossRefPubMedGoogle Scholar
  48. Striker GG, Insausti P, Grimoldi AA, Ploschuk EL, Vasellati V (2005) Physiological and anatomical basis of differential tolerance to soil flooding of Lotus corniculatus L. and Lotus glaber Mill. Plant Soil 276(1):301–311.  https://doi.org/10.1007/s11104-005-5084-0 CrossRefGoogle Scholar
  49. Striker GG, Insausti P, Grimoldi AA (2008) Flooding effects on plants recovering from defoliation in Paspalum dilatatum and Lotus tenuis. Ann Bot 102(2):247–254.  https://doi.org/10.1093/aob/mcn083 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Szczyglowski K, Stougaard J (2008) Lotus genome: pod of gold for legume research. Trends Plant Sci 13(10):515–517.  https://doi.org/10.1016/j.tplants.2008.08.001 CrossRefPubMedGoogle Scholar
  51. Taylor NL (2008) A century of clover breeding developments in the United States. Crop Sci 48(1):1–13.  https://doi.org/10.2135/cropsci2007.08.0446 CrossRefGoogle Scholar
  52. Thudi M, Upadhyaya HD, Rathore A, Gaur PM, Krishnamurthy L, Roorkiwal M, Nayak SN, Chaturvedi SK, Basu PS, Gangarao NVPR, Fikre A, Kimurto P, Sharma PC, Sheshashayee MS, Tobita S, Kashiwagi J, Ito O, Killian A, Varshney RK (2014) Genetic dissection of drought and heat tolerance in chickpea through genome-wide and candidate gene-based association mapping approaches. PLoS ONE 9(5):e96758.  https://doi.org/10.1371/journal.pone.0096758 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Udvardi MK, Tabata S, Parniske M, Stougaard J (2005) Lotus japonicus: legume research in the fast lane. Trends Plant Sci 10(5):222–228.  https://doi.org/10.1016/j.tplants.2005.03.008 CrossRefPubMedGoogle Scholar
  54. Zhu J-K (2016) Abiotic stress signaling and responses in plants. Cell 167(2):313–324.  https://doi.org/10.1016/j.cell.2016.08.029 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Zhu H, Choi H-K, Cook DR, Shoemaker RC (2005) Bridging Model and Crop Legumes through Comparative Genomics. Plant Physiol 137(4):1189–1196.  https://doi.org/10.1104/pp.104.058891 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Centro Regional de Investigación QuilamapuInstituto de Investigaciones Agropecuarias INIAChillánChile
  2. 2.Facultad de Agronomía, Departamento de Suelos y Recursos NaturalesUniversidad de ConcepciónChillánChile
  3. 3.Monsanto CompanySt. LouisUSA
  4. 4.School of Forest Resources and ConservationUniversity of FloridaGainesvilleUSA

Personalised recommendations