Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Identification of QTLs for shoot and root growth under ionic–osmotic stress in Lotus, using a RIL population

Gastón Quero A , Lucía Gutíerrez B , Ramiro Lascano C D , Jorge Monza A , Niels Sandal E and Omar Borsani A F
+ Author Affiliations
- Author Affiliations

A Laboratorio de Bioquímica, Facultad de Agronomía, Universidad de la República, Av. Garzón 780, 12900. Montevideo, Uruguay.

B Departamento de Biometría, Estadística y Computación, Facultad de Agronomía, Universidad de la República, Av. Garzón 780, 12900. Montevideo, Uruguay.

C Instituto de Fisiología y Recursos Genéticos Vegetales CIAP-INTA, Camino 60 Cuadras km 5 (X5020ICA), Córdoba, Argentina.

D Cátedra de Fisiología Vegetal. Universidad Nacional de Córdoba, Av. Vélez Sarsfield 290, 5000. Córdoba, Argentina.

E Centre for Carbohydrate Recognition and Signalling, Department of Molecular Biology and Genetics, Aarhus University, Gustav Wieds Vej 10, DK-8000 Aarhus C, Denmark.

F Corresponding author. Email: oborsani@fagro.edu.uy

Crop and Pasture Science 65(2) 139-149 https://doi.org/10.1071/CP13222
Submitted: 24 June 2013  Accepted: 19 December 2013   Published: 20 February 2014

Abstract

The genus Lotus includes a group of forage legume species including genotypes of agronomic interest and model species. In this work, an experimental hydroponic growth system allowed the discrimination of growth responses to ionic–osmotic stress in a population of recombinant inbred lines (RILs) developed from L. japonicus × L. burttii and the identification of the associated quantitative trait loci (QTLs). The analyses led to the identification of eight QTLs: three for shoot growth localised on chromosome 3, 5 and 6; one for root growth on chromosome 1; three for total growth on chromosome 1, 4 and 5; and one associated with shoot/root ratio on chromosome 3. An interaction of QTL × stress condition was established and the effect of the environment quantified. In summary, it was established that the allele from L. burttii explained most responses to osmotic stress, while the alleles of L. japonicus explained the responses related to ionic stress conditions. Of 49 markers linked to all QTLs identified, 41 expressed superiority of the L. burttii parental allele in the osmotic stress condition, but when an iso-osmotic concentration of NaCl was applied, L. burttii lost superiority in 21 of these markers. This shows the superiority of the L. japonicus parental allele in ionic stress conditions. This study is the first report in which a RIL population of lotus is analysed with the aim of providing molecular markers associated with plant responses to ionic or osmotic stress.

Additional keywords: hydroponic growth, L. japonicus, L. burttii, PEG stress, salt stress.


References

Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics International 11, 36–42.

Agbicodo EM, Fatokun CA, Muranaka S, Visser RGF, van der Linden CG (2009) Breeding drought tolerant cowpea: constraints, accomplishments, and future prospects. Euphytica 167, 353–370.
Breeding drought tolerant cowpea: constraints, accomplishments, and future prospects.Crossref | GoogleScholarGoogle Scholar |

Arbaoui M, Link W, Satovic Z, Torres A (2008) Quantitative trait loci of frost tolerance and physiologically related trait in faba bean (Vicia faba L.). Euphytica 164, 93–104.
Quantitative trait loci of frost tolerance and physiologically related trait in faba bean (Vicia faba L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFOltbnE&md5=58efdbcd8b8d9f0e9f17c0eb99a73101CAS |

Ashraf M (2010) Inducing drought tolerance in plants : Recent advances. Biotechnology Advances 28, 169–183.
Inducing drought tolerance in plants : Recent advances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGrtL3K&md5=3fb25c64c0c392583ce99a074be82ddaCAS | 19914371PubMed |

Athar HR, Ashraf M (2009) Strategies for crop improvement against salinity and drought stress : An overview. In ‘Salinity and water stress: Improving crop efficiency’. (Eds M Ashraf, M Ozturk, HR Athar) pp. 1–16. (Springer: Osnabrueck, Germany)

Bates D, Maechler M (2010) lme4: Linear mixed-effects models. R package version 0.999375-37/r1127. R-Forge. http://R-Forge.R-project.org/projects/lme4/

Boer MP, Wright D, Feng L, Podlich DW, Luo L, Cooper M, van Eeuwijk FA (2007) A mixed-model quantitative trait loci (QTL) analysis for multiple-environment trial data using environmental covariables for QTL-by-environment interactions, with an example in maize. Genetics 177, 1801–1813.
A mixed-model quantitative trait loci (QTL) analysis for multiple-environment trial data using environmental covariables for QTL-by-environment interactions, with an example in maize.Crossref | GoogleScholarGoogle Scholar | 17947443PubMed |

Bonnin I, Prosperi J, Olivierit I (1996) Genetic markers and quantitative genetic variation in Medicago truncutula (Leguminosae): A comparative analysis of population structure. Genetics 143, 1795–1805.

Bonnin I, Prosperi JM, Olivieri I (1997) Comparison of quantitative genetic parameters between two natural populations of a selfing plant species, Medicago truncatula Gaertn. Theoretical and Applied Genetics 94, 641–651.
Comparison of quantitative genetic parameters between two natural populations of a selfing plant species, Medicago truncatula Gaertn.Crossref | GoogleScholarGoogle Scholar |

Borsani O, Cuartero J, Fernández JA, Valpuesta V, Botella MA (2001) Identification of two loci in tomato reveals distinct mechanisms for salt tolerance. The Plant Cell 13, 873–887.

Borsani O, Valpuesta V, Botella MA (2003) Developing salt tolerant plants in a new century: a molecular biology. Plant Cell, Tissue and Organ Culture 73, 101–115.
Developing salt tolerant plants in a new century: a molecular biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1Kitrs%3D&md5=665fe3ff87238eb9e28c060294b4ea24CAS |

Botella MA, Rosado A, Bressan RA, Hasegawa PM (2005) Plant adaptive responses to salinity stress. In ‘Plant abiotic stress’. (Ed. A Matthew) pp. 38–62. (Blackwell Publishing: Oxford, UK)

Bouteillé M, Rolland G, Balsera C, Loudet O, Muller B (2012) Disentangling the intertwined genetic bases of root and shoot growth in Arabidopsis. PLoS ONE
Disentangling the intertwined genetic bases of root and shoot growth in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 22384215PubMed |

Broman KW, Sen S (2009) Data checking. In ‘A guide to QTL mapping with R/qtl’. (Eds M Gail, K Krickeberg, J Samet, A Tsiatis, W Wong) pp. 47–73. (Springer: New York)

Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl : QTL mapping in experimental crosses. Bioinformatics 19, 889–890.
R/qtl : QTL mapping in experimental crosses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVKmtb0%3D&md5=8681c6c6e6e3f82bcded8423770e88c4CAS | 12724300PubMed |

Cogan N, Abberton M, Smith K, Kearney G, Marshall A, Williams A, Michaelson-Yeates T, Bowen C, Jones E, Vecchies A, Forster J (2006) Individual and multi-environment combined analyses identify QTLs for morphogenetic and reproductive development traits in white clover (Trifolium repens L.). Theoretical and Applied Genetics 112, 1401–1415.
Individual and multi-environment combined analyses identify QTLs for morphogenetic and reproductive development traits in white clover (Trifolium repens L.).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283ntVamsw%3D%3D&md5=c2104fd1e5783793d15c385446ab6c25CAS | 16699790PubMed |

Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: The basic concepts. Euphytica 142, 169–196.
An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: The basic concepts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvVWjs7c%3D&md5=38a9786c7f07da4824e15b291825a663CAS |

Collins N, Tardieu F, Tuberosa R (2008) Quantitative trait loci and crop performance under abiotic stress : Where do we stand? Plant Physiology 147, 469–486.
Quantitative trait loci and crop performance under abiotic stress : Where do we stand?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVyhsbw%3D&md5=48d814a451b7e894ee249543fe918223CAS | 18524878PubMed |

Cuartero J, Bolarín MC, Asíns MJ, Moreno V (2006) Increasing salt tolerance in the tomato. Journal of Experimental Botany 57, 1045–1058.
Increasing salt tolerance in the tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Glsrc%3D&md5=d98d8bcd0bc30d18107aa6e94a041a0aCAS | 16520333PubMed |

Díaz P, Monza J, Márquez A (2005) Drought and saline stress in Lotus japonicus. In ‘Lotus japonicus handbook’. (Ed. AJ Márquez) pp. 39–50. (Springer: Dordrecht, the Netherlands)

Flowers TJ (2004) Improving crop salt tolerance. Journal of Experimental Botany 55, 307–319.
Improving crop salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1egtQ%3D%3D&md5=73baa51874b27fb318bacc1147213fb8CAS | 14718494PubMed |

Gondo T, Sato S, Okumura K, Tabata S, Akashi R, Sachiko I (2007) Quantitative trait locus analysis of multiple agronomic traits in the model legume Lotus japonicus. Genome 50, 627–637.
Quantitative trait locus analysis of multiple agronomic traits in the model legume Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 17893740PubMed |

Handberg K, Stougaard J (1992) Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. The Plant Journal 2, 487–496.
Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics.Crossref | GoogleScholarGoogle Scholar |

Hayashi M, Miyahara A, Sato S, Kato T, Yoshikawa M, Taketa M, Hayashi M, Pedrosa A, Onda R, Imaizumi-Anraku H, Bachmair A, Sandal 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 F2 population. DNA Research 8, 301–310.
Construction of a genetic linkage map of the model legume Lotus japonicus using an intraspecific F2 population.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFGhsLg%3D&md5=531c26958ed98e16892fb5c0ee803c2bCAS | 11853317PubMed |

Kawaguchi M, Pedrosa-Harand A, Yano K, Hayashi M, Murooka Y, Saito K, Nagata T, Namai K, Nishida H, Shibata D, Sato S, Tabata S, Hayashi M, Harada K, Sandal N, Stougaard J, Bachmair A, Grant WF (2005) Lotus burttii takes a position of the third corner in the Lotus. DNA Research 12, 69–77.
Lotus burttii takes a position of the third corner in the Lotus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktFKqsLw%3D&md5=bc9a4d18b51beaa9c97bc3d1d2b10008CAS | 16106754PubMed |

Khan HR, Paull JG, Siddique KHM, Stoddard FL (2010) Faba bean breeding for drought-affected environments: A physiological and agronomic perspective. Field Crops Research 115, 279–286.
Faba bean breeding for drought-affected environments: A physiological and agronomic perspective.Crossref | GoogleScholarGoogle Scholar |

Loudet O, Gaudon V, Trubuil A, Daniel-Vedele F (2005) Quantitative trait loci controlling root growth and architecture in Arabidopsis thaliana confirmed by heterogeneous inbred family. Theoretical and Applied Genetics 110, 742–753.
Quantitative trait loci controlling root growth and architecture in Arabidopsis thaliana confirmed by heterogeneous inbred family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsFShurg%3D&md5=0637b7a9f4d9a1771a3b7c786f2a5183CAS | 15678326PubMed |

Mackay TFC, Stone EA, Ayroles JF (2009) The genetics of quantitative traits: challenges and prospects. Nature Reviews. Genetics 10, 565–577.
The genetics of quantitative traits: challenges and prospects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXos1WjsL0%3D&md5=ca274a59b74bdb8b65c91ab0e44818a8CAS |

Malosetti M, Voltas J, Romagosa I, Ullrich SE, van Eeuwijk FA (2004) Mixed models including environmental covariables for studying QTL by environment interaction. Euphytica 137, 139–145.
Mixed models including environmental covariables for studying QTL by environment interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntlekur0%3D&md5=27910954e8e32967957044ffcbf1175fCAS |

Malosetti M, van Eeuwijk FA, Boer MP, Casas AM, Elía M, Moralejo M, Bhat PR, Ramsay L, Molina-Cano JL (2011) Gene and QTL detection in a three-way barley cross under selection by a mixed model with kinship information using SNPs. Theoretical and Applied Genetics 122, 1605–1616.
Gene and QTL detection in a three-way barley cross under selection by a mixed model with kinship information using SNPs.Crossref | GoogleScholarGoogle Scholar | 21373796PubMed |

Margarido GRA, Souza AP, Garcia AAF (2007) OneMap : software for genetic mapping in outcrossing species. Hereditas 144, 78–79.
OneMap : software for genetic mapping in outcrossing species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2svks1GhtA%3D%3D&md5=17042c7e17ad058996b3c55d9c6a3cbeCAS |

Melchiorre M, Quero GE, Parola R, Racca R, Trippi VS, Lascano R (2009) Physiological characterization of four model Lotus diploid genotypes: L. japonicus (MG20 and Gifu), L. filicaulis, and L. burttii under salt stress. Plant Science 177, 618–628.
Physiological characterization of four model Lotus diploid genotypes: L. japonicus (MG20 and Gifu), L. filicaulis, and L. burttii under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1OrurjM&md5=57be8c5b75e893f071522e517e5b0d02CAS |

Miflin B (2000) Crop improvement in the 21st century. Journal of Experimental Botany 51, 1–8.
Crop improvement in the 21st century.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXpslGquw%3D%3D&md5=7ac9494661853ae0268b49a30b80b8f0CAS | 10938790PubMed |

Milne I, Shaw P, Stephen G, Bayer M, Cardle L, Thomas WTB, Flavell AJ, Marshall D (2010) Flapjack graphical genotype visualization. Bioinformatics 26, 3133–3134.
Flapjack graphical genotype visualization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFamtr%2FN&md5=b76c70fcf69d5cc4f0f98903bd44929aCAS | 20956241PubMed |

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
Comparative physiology of salt and water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhslakurw%3D&md5=d37d9dcaf3bd97d4394253d702ae8df7CAS |

Munns R (2009) Strategies for crop improvement in saline soils. In ‘Salinity and water stress: Improving crop efficiency’. (Eds M Ashraf, MÑ Ozturk, HR Athar) pp. 99–110. (Springer: Osnabrueck, Germany)

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=2ae0a0853b4c70882fd18e1200943485CAS | 18444910PubMed |

Munns R, Husain S, Rivelli AR, Condon AG, James RA, Lindsay MP, Lagudah ES, Schachtman DP, Hare RA (2002) Avenues for increasing salt tolerance of crops, and the role of physiologically based selection traits. Plant and Soil 247, 93–105.
Avenues for increasing salt tolerance of crops, and the role of physiologically based selection traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVCmu7k%3D&md5=ca817a70909da546be5d94796d4d7144CAS |

Ohmido N, Ishimaru A, Kato S, Sato S, Tabata S, Fukui K (2010) Integration of cytogenetic and genetic linkage maps of Lotus japonicus, a model plant for legumes. Chromosome Research 18, 287–299.
Integration of cytogenetic and genetic linkage maps of Lotus japonicus, a model plant for legumes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjslGksL4%3D&md5=ade5e1c67d159f4189260021d7239a7eCAS | 20076998PubMed |

Pedrosa A, Sandal N, Stougaard J, Schweizer D, Bachmair A (2002) Chromosomal map of the model legume Lotus japonicus. Genetics 161, 1661–1672.

Salekdeh GH, Reynolds M, Bennett J, Boyer J (2009) Conceptual framework for drought phenotyping during molecular breeding. Trends in Plant Science 14, 488–496.
Conceptual framework for drought phenotyping during molecular breeding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2lurnK&md5=74dbe10257635d6b546b8c983b83066fCAS | 19716744PubMed |

Sandal N, Krusell L, Radutoiu S, Olbryt M, Pedrosa A, Bachmair A, Ketelsen T, Stracke S, Sato S, Kato T, Parniske M, Tabata S, Stougaard J (2002) A genetic linkage map of the model legume Lotus japonicus and strategies for fast mapping of new loci. Genetics 161, 1673–1683.

Sandal N, Petersen TR, Murray J, Umehara Y, Karas B, Yano K, Kumagai H, Yoshikawa M, Saito K, Hayashi M, Murakami Y, Wang X, Hakoyama T, Imaizumi-Anraku H, Sato S, Kato T, Chen W, Hossain MS, Shibata S, Wang TL, Yokota K, Larsen K, Kanamori N, Madsen E, Radutoiu S, Madsen LH, Radu TG, Krusell L, Ooki Y, Banba M, Betti M, Rispail N, Skøt L, Tuck E, Perry J, Yoshida S, Vickers K, Pike J, Mulder L, Charpentier M, Müller J, Ohtomo R, Kojima T, Ando S, Marquez AJ, Gresshoff PM, Harada K, Webb J, Hata S, Suganuma N, Kouchi H, Kawasaki S, Tabata S, Hayashi M, Parniske M, Szczyglowski K, Kawaguchi M, Stougaard J (2006) Genetics of symbiosis in Lotus japonicus: Recombinant inbred lines, comparative genetic maps, and map position of 35 symbiotic loci. Molecular Plant-Microbe Interactions 19, 80–91.
Genetics of symbiosis in Lotus japonicus: Recombinant inbred lines, comparative genetic maps, and map position of 35 symbiotic loci.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisVWjtw%3D%3D&md5=ae3f15a9d0409ec582c84179c0e1e2eeCAS | 16404956PubMed |

Sandal N, Jin H, Rodriguez-Navarro DN, Temprano F, Cvitanich C, Brachmann A, Sato S, Kawaguchi M, Tabata S, Parniske M, Ruiz-sainz JE, Andersen SU, Stougaard J (2012) A set of Lotus japonicus Gifu × Lotus burttii recombinant inbred lines facilitates map-based cloning and QTL mapping. DNA Research 19, 317–323.
A set of Lotus japonicus Gifu × Lotus burttii recombinant inbred lines facilitates map-based cloning and QTL mapping.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFOku7bI&md5=d4d9ed91d111bb95b846e38addf327b0CAS | 22619310PubMed |

Sato S, Tabata S (2006) Lotus japonicus as a platform for legume research. Current Opinion in Plant Biology 9, 128–132.
Lotus japonicus as a platform for legume research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhvVWrtbo%3D&md5=b66ab91377d524e79e2fd1ac18941acaCAS | 16480917PubMed |

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 Research 15, 227–239.
Genome structure of the legume, Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12ht7zO&md5=6ac76a85a719032a1f4ca9f2d60ae528CAS | 18511435PubMed |

Stougaard J, Beuselinck PR (1996) Registration of GIFU B-129-S9 Lotus japonicus germplasm. Crop Science 36, 476
Registration of GIFU B-129-S9 Lotus japonicus germplasm.Crossref | GoogleScholarGoogle Scholar |

Tanksley SD (1993) Mapping polygenes. Annual Review of Genetics 27, 205–233.
Mapping polygenes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXht1KitLc%3D&md5=b4785034e513a0bb41be752ce0310e68CAS | 8122902PubMed |

Tuberosa R, Salvi S, Sanguineti MC, Landi P, Maccaferri M, Conti S (2002) Mapping QTLs regulating morpho-physiological traits and yield : Case studies, shortcomings and perspectives in drought-stressed maize. Annals of Botany 89, 941–963.
Mapping QTLs regulating morpho-physiological traits and yield : Case studies, shortcomings and perspectives in drought-stressed maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVeitb8%3D&md5=b8d833e632341e104d9ba89da6bd0f2dCAS | 12102519PubMed |

Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. The Plant Journal 45, 523–539.
Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XislWit7w%3D&md5=586950a0ede592ff02dba9bbf606b4caCAS | 16441347PubMed |

Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures : towards genetic engineering for stress tolerance. Planta 218, 1–14.
Plant responses to drought, salinity and extreme temperatures : towards genetic engineering for stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovV2ltbo%3D&md5=b41c3759228be05f2bd4140c0250a535CAS | 14513379PubMed |

Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants : challenges and opportunities. Trends in Plant Science 10, 615–620.
Developing salt-tolerant crop plants : challenges and opportunities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Oms7%2FI&md5=be6f8ca1e57d4acbd6b7f715b3f6b9d3CAS | 16280254PubMed |

Young ND, Cannon SB, Sato S, Kim D, Cook DR, Town CD, Roe BA, Tabata S (2005) Sequencing the genespaces of Medicago truncatula and Lotus japonicus. Plant Physiology 137, 1174–1181.
Sequencing the genespaces of Medicago truncatula and Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslaqtbo%3D&md5=6ece5d8e252db651b9aa8539ca0963baCAS | 15824279PubMed |