Log in

Quantitative trait loci analysis of morphological traits in Citrus

  • Original Article
  • Published:
Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

The objectives of this study were to understand the genetic basis of morphological variation observed in the genus Citrus and its relatives and to identify genomic regions associated with certain morphological traits using genetic linkage map** and quantitative trait loci (QTLs) analysis with random amplified polymorphic DNA (RAPD) markers. First, a genetic linkage map was constructed with RAPD markers obtained by screening 98 progeny plants from a {Citrus grandis × [C. paradisi × Poncirus trifoliata]} × {[(C. paradisi × P. trifoliata) × C. reticulata] × [(C. paradisi × Poncirus trifoliata) × C. sinensis]} intergeneric cross. The map contains 69 RAPD markers distributed into nine linkage groups. Then, 17 different morphological traits, including six tree and two leaf characters of 98 progeny plants and six floral and three fruit characters of about half of the same progeny plants were evaluated for 2 years and statistically analyzed for variation. Statistical analysis of individual traits indicated that trunk diameter and growth, tree height, canopy width, tree vigor and growth, leaf length and width, petal and anther numbers, petal length and width, length of pistil and style, fruit length and diameter, and fruit segment number showed normal or close to normal distribution, suggesting that these traits may be inherited quantitatively. Quantitative data from the morphological traits were analyzed to detect markers and putative QTLs associated with these traits using interval map** method. QTL analysis revealed 18 putative QTLs of LOD > 3.0 associated with 13 of the morphological traits analyzed. The putative QTLs were distributed in several different linkage groups, and QTLs associated with similar traits were mostly mapped to the same LG or similar locations in the linkage group, indicating that the same genomic region is involved in the inheritance of some of the morphological traits.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abdel-Haleem H, Lee GJ, Boerma RH (2011) Identification of QTL for increased fibrous roots in soybean. Theor Appl Genet 122(5):935–946

    Article  PubMed  Google Scholar 

  • Asins MJ, Bernet GP, Ruiz C, Cambra M, Guerri J, Carbonell EA (2004) QTL analysis of Citrus tristeza virus-citradia interaction. Theor Appl Genet 108:603–611

    Article  PubMed  CAS  Google Scholar 

  • Benter T, Papadopoulos S, Pape M, Manns M, Poliwoda H (1995) Optimization and reproducibility of random amplified polymorphic DNA in humans. Anal Biochem 230:92–100

    Article  PubMed  CAS  Google Scholar 

  • Bernet GP, Margaix C, Jacas J, Carbonell EA, Asins MJ (2005) Genetic analysis of citrus leafminer susceptibility. Theor Appl Genet 110:1393–1400

    Article  PubMed  CAS  Google Scholar 

  • Cai Q, Guy CL, Moore GA (1994) Extension of the linkage map in Citrus using random amplified polymorphic DNA (RAPD) markers and RFLP map** of cold-acclimation responsive loci. Theor Appl Genet 89:606–614

    Article  CAS  Google Scholar 

  • Cameron JW, Frost HB (1968) Genetics, breeding, and nucellar embryony. In: Reuther W, Batchelor LD, Webber HJ (eds) The citrus industry. Division of Agricultural Sciences, University of California, Riverside, pp 325–370

    Google Scholar 

  • Cameron JW, Soost RK (1980) Leaf types of F1 hybrids and backcrosses involving unifoliate Citrus and trifoliate Poncirus. J Am Soc Hortic Sci 105:517–519

    Google Scholar 

  • Caranta C, Palloix A, Lefebvre V, Daubeze AM (1997) QTLs for a component of partial resistance to cucumber mosaic virus in pepper: restriction of virus installation in host cells. Theor Appl Genet 94:431–438

    Article  CAS  Google Scholar 

  • Cerqueira-Silva CB, Cardoso-Silva CB, Santos ES, Conceição LD, Pereira AS, Oliveira AC, Corrêa RX (2010) Genetic diversity in wild species of passion fruit (Passiflora trintae) based on molecular markers. Genet Mol Res 26 9(4):2123–2130

    CAS  Google Scholar 

  • Cheng FC, Roose ML (1995) Origin and inheritance of dwarfing by the citrus rootstock Poncirus trifoliata cv. Flying Dragon. J Am Soc Hortic Sci 120:286–291

    Google Scholar 

  • Cheng Y, Geng J, Zhang J, Wang Q, Ban Q, Hou X (2009) The construction of a genetic linkage map of non-heading Chinese cabbage (Brassica campestris ssp. chinensis Makino). J Genet Genomics 36(8):501–508

    Article  PubMed  CAS  Google Scholar 

  • Deng ZN, Gentile A, Nicolosi E, Domina F, Vardi A, Tribulato E (1995) Identification of in vivo and in vitro lemon mutants by RAPD markers. J Hortic Sci 70:117–125

    CAS  Google Scholar 

  • Douhan GW, Smith ME, Huyrn KL, Westbrook A, Beerli P, Fisher AJ (2008) Multigene analysis suggests ecological speciation in the fungal pathogen Claviceps purpurea. Mol Ecol 17(9):2276–2286

    Article  PubMed  CAS  Google Scholar 

  • Durham RE, Liou PC, Gmitter FG Jr, Moore GA (1992) Linkage of restriction fragment length polymorphisms and isozymes in citrus. Theor Appl Genet 84:39–48

    Article  CAS  Google Scholar 

  • Edwards KJ, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 19:1349–1355

    Google Scholar 

  • Fang DQ, Federici CT, Roose ML (1997) Development of molecular markers linked to a gene controlling fruit acidity in citrus. Genome 40(6):841–849

    Article  PubMed  CAS  Google Scholar 

  • Fani R, Damiani G, Di SC, Gallori E et al (1993) Use of random amplified polymorphic DNA (RAPD) for generating specific DNA probes for microorganisms. Mol Ecol 2:243–250

    Google Scholar 

  • Finger FL, Lannes SD, Schuelter AR, Doege J, Comerlato AP, Gonçalves LS, Ferreira FR, Clovis LR, Scapim CA (2010) Genetic diversity of Capsicum chinensis (Solanaceae) accessions based on molecular markers and morphological and agronomic traits. Genet Mol Res 21 9(3):1852–1864

    Article  CAS  Google Scholar 

  • Foolad MR, Chen FQ (1998) RAPD markers associated with salt tolerance in an interspecific crosses of tomato (Lycopersicon esculentum x L pennellii). Plant Cell Rep 17:306–312

    Article  CAS  Google Scholar 

  • Garcia MR, Asins MC, Carbonell EA (2000) QTL analysis of yield and seed number of Citrus. Theor Appl Genet 101:487–493

    Article  CAS  Google Scholar 

  • Gelderman H (1975) Investigations on inheritance of quantitative characters in animals by gene markers. Theor Appl Genet 46:319–330

    Article  Google Scholar 

  • Genc Y, Oldach K, Verbyla AP, Lott G, Hassan M, Tester M, Wallwork H, McDonald GK (2010) Sodium exclusion QTL associated with improved seedling growth in bread wheat under salinity stress. Theor Appl Genet 121(5):877–894

    Article  PubMed  CAS  Google Scholar 

  • Gmitter FG Jr, Grosser JW, Moore GA (1992) Citrus. In: Hammerschlag FA, Litz RE (eds) Biotechnology of perennial fruit crops. CAB International, Wallingford, pp 335–369

    Google Scholar 

  • González C, Camacho MV, Benito C (2002) Chromosomal location of 46 new RAPD markers in rye (Secale cereale L.). Genetica 115(2):205–211

    Article  PubMed  Google Scholar 

  • Gostimsky SA, Kokaeva ZG, Konovalov FA (2005) Studying plant genome variation using molecular markers. Russ J Genet 41:378–388

    Google Scholar 

  • Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: map** strategy and RAPD markers. Genetics 137:1121–1137

    PubMed  CAS  Google Scholar 

  • Gyenis L, Yun SJ, Smith KP, Steffenson BJ, Bossolini E, Sanguineti MC, Muehlbauer GJ (2007) Genetic architecture of quantitative trait loci associated with morphological and agronomic trait differences in a wild by cultivated barley cross. Genome 50(8):714–723

    Article  PubMed  CAS  Google Scholar 

  • Hao YJ, Wen XP, Deng XX (2004) Genetic and epigenetic evaluations of citrus calluses recovered from slow-growth culture. J Plant Physiol 161(4):479–484

    Article  PubMed  CAS  Google Scholar 

  • James CM, Clarke JB, Evans KM (2004) Identification of molecular markers linked to the mildew resistance gene Pl-d in apple. Theor Appl Genet 110:175–181

    Article  PubMed  CAS  Google Scholar 

  • Jarrell DC, Roose ML, Traugh SN, Kupper RS (1992) A genetic map of citrus based on the segregation of isozymes and RFLPs in an intergeneric cross. Theor Appl Genet 84:49–56

    Article  CAS  Google Scholar 

  • Kennard WC, Havey MJ (1995) Quantitative trait analysis of fruit quality in cucumber: QTL detection, confirmation, and comparison with mating-design variation. Theor Appl Genet 91:53–61

    Google Scholar 

  • Khowaja FS, Norton GJ, Courtois B, Price AH (2009) Improved resolution in the position of drought-related QTLs in a single map** population of rice by meta-analysis. BMC Genomics 10:276

    Article  PubMed  Google Scholar 

  • Kijas JMH, Fowler JCS, Garbett CA, Thomas MR (1995) An evaluation of sequence tagged microsatellite markers for genetic analysis within Citrus and related species. Genome 38:349–355

    Article  PubMed  CAS  Google Scholar 

  • Kijas JMH, Thomas MR, Fowler JCS, Roose ML (1997) Integration of trinucleotide microsatellites into a linkage map of Citrus. Theor Appl Genet 94:701–706

    Article  CAS  Google Scholar 

  • Lee YC, Yang VC, Wang TS (2007) Use of RAPD to detect sodium arsenite-induced DNA damage in human lymphoblastoid cells. Toxicology 239(1–2):108–115

    Article  PubMed  CAS  Google Scholar 

  • Ling P, Duncan LW, Deng ZB, Dunn D, Hu X, Huang S, Gmitter FG Jr (2000) Inheritance of citrus nematode resistance and its linkage with molecular markers. Theor Appl Genet 100:1010–1017

    Article  CAS  Google Scholar 

  • Liou PC (1990) A molecular study of the Citrus genome through analysis of restriction fragment length polymorphism and isozyme map**. PhD thesis. University of Florida, Gainesville

  • Mian MAR, Ashley DA, Boerma HR (1998) An additional QTL for water use efficiency in soybean. Crop Sci 38:390–393

    Article  Google Scholar 

  • Mohan M, Nair S, Bhagwat A, Krishna TG, Yano M, Bhatia CR, Sasaki T (1997) Genome map**, molecular markers and marker-assisted selection in crop plants. Mol Breed 3:87–103

    Article  CAS  Google Scholar 

  • Moreno E, Obando JM, Dos-Santos N, Fernández-Trujillo JP, Monforte AJ, Garcia-Mas J (2008) Candidate genes and QTLs for fruit ripening and softening in melon. Theor Appl Genet 116:589–602

    Article  PubMed  CAS  Google Scholar 

  • Orr W, Molnar SJ (2008) Development of PCR-based SCAR and CAPS markers linked to beta-glucan and protein content QTL regions in oat. Genome 51(6):421–425

    Article  PubMed  CAS  Google Scholar 

  • Paran I, Goldman I, Zamir D (1997) QTL analysis of morphological traits in a tomato recombinant inbred line population. Genome 40:242–248

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Lander ES, Hewitt JD, Peterson S, Lincoln SE, Tanksley SD (1988) Resolution of quantitative traits into Mendelian factors using a complete linkage map of restriction fragment length polymorphisms. Nature 335:721–726

    Article  PubMed  CAS  Google Scholar 

  • Pérez-Vega E, Pañeda A, Rodríguez-Suárez C, Campa A, Giraldez R, Ferreira JJ (2010) Map** of QTLs for morpho-agronomic and seed quality traits in a RIL population of common bean (Phaseolus vulgaris L.). Theor Appl Genet 120(7):1367–1380

    Article  PubMed  Google Scholar 

  • Raina RM, Rani SN, Kojima V, Ogihara T, Singh Y, Devarumath KP (2001) RAPD and ISSR fingerprints as useful genetic markers for analysis of genetic diversity, varietal identification, and phylogenetic relationships in peanut (Arachis hypogaea) cultivars and wild species. Genome 44:763–772

    PubMed  CAS  Google Scholar 

  • Russo G, Fanizza G (1992) Genotypic variability and interrelationship among morphological and biochemical fruit characters in mandarins. Proc Int Soc Citric 1:96–97

    Google Scholar 

  • Schoenenberger N, Felber F, Savova-Bianchi D, Guadagnuolo R (2005) Introgression of wheat DNA markers from A, B and D genomes in early generation progeny of Aegilops cylindrica Host × Triticum aestivum L. hybrids. Theor Appl Genet 111(7):1338–1346

    Article  PubMed  CAS  Google Scholar 

  • Siviero A, Cristofani M, Furtado EL, Garcia AA, Coelho AS, Machado MA (2006) Identification of QTLs associated with citrus resistance to Phytophthora gummosis. J Appl Genet 47:23–28

    Article  PubMed  Google Scholar 

  • Soost RK, Cameron JW (1975) Citrus. In: Janick JM, Moore JN (eds) Advances in fruit breeding. Purdue University Press, West Lafayette, pp 507–540

    Google Scholar 

  • Soost RK, Roose ML (1996) Citrus. In: Janick JM, Moore JN (eds) Fruit breeding. Wiley, New York, pp 257–323

    Google Scholar 

  • Souza EA, Camargo OA Jr, Pinto JM (2010) Sexual recombination in Colletotrichum lindemuthianum occurs on a fine scale. Genet Mol Res 9(3):1759–1769

    Article  PubMed  CAS  Google Scholar 

  • Stam P, Van Ooijen JW (1995) JoinMap (TM) version 20: software for the calculation of genetic linkage maps. Version 2.0 ed CPRO-DLO, Wageningen

  • Tondelli AFE, Barabaschi D, April A, Skinner JS, Stockinger EJ, Stanca AM, Pecchioni N (2006) Map** regulatory genes as candidates for cold and drought stress tolerance in barley. Theor Appl Genet 112:445–454

    Article  PubMed  CAS  Google Scholar 

  • Tozlu I, Guy CL, Moore GA (1999a) QTL analysis of Na and Cl accumulation related traits in an intergeneric BC1 progeny of Citrus and Poncirus under saline and nonsaline environments. Genome 42:692–705

    CAS  Google Scholar 

  • Tozlu I, Guy CL, Moore GA (1999b) QTL analysis of morphological traits in an intergeneric BC1 progeny of Citrus and Poncirus under saline and nonsaline environments. Genome 42:1020–1029

    CAS  Google Scholar 

  • Van Ooijen JW, Maliepaard C (1996) MapQTL (TM) version 30 software for the calculation of QTL positions on genetic maps. Version 3.0 ed CPRO-DLO, Wageningen

  • Vega AE, Cortiñas TI, Puig ON, Silva HJ (2010) Molecular characterization and susceptibility testing of Helicobacter pylori strains isolated in western Argentina. Int J Infect Dis 14[Suppl 3]:e85–e92

    Article  PubMed  Google Scholar 

  • Venkatachalam L, Sreedhar RV, Bhagyalakshmi N (2008) The use of genetic markers for detecting DNA polymorphism, genotype identification and phylogenetic relationships among banana cultivars. Mol Phylogenet Evol 47:974–985

    Article  PubMed  CAS  Google Scholar 

  • Villalta I, Reina-Sánchez A, Bolarín MC, Cuartero J, Belver A, Venema K, Carbonell EA, Asins MJ (2008) Genetic analysis of Na(+) and K (+) concentrations in leaf and stem as physiological components of salt tolerance in Tomato. Theor Appl Genet 16:869–880

    Article  Google Scholar 

  • Weber CA, Moore GA, Deng Z, Gmitter FG Jr (2003) Map** freeze tolerance quantitative trait loci in a Citrus grandis × Poncirus trifoliata F1 pseudo-testcross using molecular markers. J Am Soc Hortic Sci 128:508–514

    CAS  Google Scholar 

  • Welsh JM, McClelland M (1990) Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Res 18:7213–7218

    Article  PubMed  CAS  Google Scholar 

  • Williams JGK, Kubelic AR, Livak KJ, Rafalski JA, Tingey SV (1990) Polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 18:6531–6535

    Article  PubMed  CAS  Google Scholar 

  • Xue DW, Chen MC, Zhou Chen S, Mao Y, Zhang H (2008) QTL analysis of flag MX, leaf in barley (Hordeum vulgare L) for morphological traits and chlorophyll content. J Zhejiang Univ Sci B 9:938–943

    Article  PubMed  Google Scholar 

  • Zhang YX, Wang Q, Jiang L, Liu LL, Wang BX, Shen YY, Cheng XN, Wan JM (2011) Fine map** of qSTV11 (KAS), a major QTL for rice stripe disease resistance. Theor Appl Genet 122(8):1591–1604

    Article  PubMed  CAS  Google Scholar 

  • Zwonitzer JC, Bubeck DM, Bhattramakki D, Goodman MM, Arellano C, Balint-Kurti PJ (2009) Use of selection with recurrent backcrossing and QTL map** to identify loci contributing to southern leaf blight resistance in a highly resistant maize line. Theor Appl Genet 118:911–925

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Courtney Weber and Antoinette Sankar for their technical assistance and F.G. Gmitter, Jr. for assistance with the software. This research project was funded in part by the Florida Citrus Production Research Advisory Council.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mehtap Şahin-Çevik.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Şahin-Çevik, M., Moore, G.A. Quantitative trait loci analysis of morphological traits in Citrus . Plant Biotechnol Rep 6, 47–57 (2012). https://doi.org/10.1007/s11816-011-0194-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-011-0194-z

Keywords

Navigation