Theoretical and Applied Genetics

, Volume 92, Issue 5, pp 599–609 | Cite as

Genetic diversity in the orange subfamily Aurantioideae. I. Intraspecies and intragenus genetic variability

  • R. Herrero
  • M. J. Asíns
  • E. A. Carbonell
  • L. Navarro


Despite the great economic importance of citrus, its phylogeny and taxonomy remain a matter of controversy. Moreover pathogens of increased virulence and dramatic environmental changes are currently spreading or emerging. The objectives of the present paper, measuring genetic variability and studying its pattern of distribution, are crucial steps to optimize sampling strategies in the search of genotypes that tolerate or resist these threatening factors within the huge array of Citrus and Citrus related species. Their intraspecific and intrageneric variability was studied comparatively by means of ten enzymatic systems using eight different measures. The analysis of ten enzymatic systems allowed us to distinguish all the species and all but one artificial hybrid. The species with the lowest genotypic variability are C. myrtifolia, C. deliciosa (willow leaf mandarin), C. paradisi (grapefruit), C. limon (lemon) and C. sinensis (sweet orange), while Severinia buxifolia shows the highest value. A broad spectrum of heterozygosity values was found in the collection. Lemons (C. limon, C. meyeri, C. karna, C. volkameriana), limes (C. aurantifolia, C. limettioides, C. lattifolia) and C. bergamia show a very high percentage of heterozygosity which indicates an origin through interspecific hybridization. Two main factors limit genetic intraspecific variability: apomictic reproduction, where nucellar embryos are much more vigorous than the zygotic ones, and nurserymen selecting against variability in the seedling stage of the rootstocks or in propagating the scion cultivars vegetatively. Additionally, self-pollination appears in some species mainly used as rootstocks which would explain their low heterozygosity values. Genetic differences between species and genera are in general high, which suggests that adaptation might have played an important role during the evolution of the orange subfamily.

Key words

Citrus Fortunella Poncirus Isozymes Genetic diversity Germ plasm bank Heterozygosity 


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  1. Almansa MS, del Rio LA, Alcaraz CF, Sevilla F (1989) Isoenzyme pattern of superoxide dismutase in different varieties of citrus plants. Physiol Plant 76:563–568Google Scholar
  2. Asíns MJ, Carbonell EA (1987) Concepts involved in measuring genetic variability and its importance in conservation of plant genetic resources. Evol Trends Plants 1:51–61Google Scholar
  3. Asíns MJ, Carbonell EA (1989) Distribution of genetic variability in a durum wheat collection. Theor Appl Genet 77:287–294Google Scholar
  4. Asíns MJ, Herrero R, Navarro L (1995) Factors affecting tree isozyme-gene expression. Theor Appl Genet 90:892–898Google Scholar
  5. Bacchi O (1943) Cytological observations in Citrus. III. Megasporogenesis, fertilization and polyembryony. Bot Gaz 105:221–225Google Scholar
  6. Barret MC, Rhodes AM (1976) A numerical taxonomic study of affinity relationships in cultivated Citrus and its close relatives. Systematic Bot 1:105–135Google Scholar
  7. Benzecri JP (1970) Distance distributionelle et metrique chi-deux en analyse factorielle des correspondences. Laboratoire de Statistique Math., ParisGoogle Scholar
  8. Bretó MP, Asíns MJ, Carbonell EA (1993) Genetic variability in Lycopersicon species and their genetic relationships. Theor Appl Genet 86:113–120Google Scholar
  9. Cameron JW, Garber MJ (1968) Identical-twin hybrids of Citrus Poncirus from strictly sexual seed parents. Amer J Bot 55:199–205Google Scholar
  10. Carpenter JB, Reece PC (1969) Catalog of genera, species and subordinate taxa in the orange subfamily Aurantoideae (Rutaceae). Agricultural Research Service ARS, USDAGoogle Scholar
  11. Castle WS (1987) Citrus rootstocks. In: Rom RC, Carlson RF (eds) Rootstocks for fruit crops. John Wiley and Sons, New York, pp 361–399Google Scholar
  12. Castle WS, Pelosi RR, Youtsey CO, Gmitter Jr, Lee RF, Powell CA, Hu X (1992) Rootstocks similar to sour orange for Florida Citrus tree. Proc Fla State Hort Soc 105:56–60Google Scholar
  13. Cavalli-Sforza LL, Edwards WF (1967) Phylogenetic analysis: models and estimation procedures. Am J Hum Genet 19:233–257Google Scholar
  14. Chao H-Y, Chiang Y-H, Chang C-B, Chiu C-S, Su W-F (1979) Distribution of seedling yellows tristeza virus in citrus and the tristeza susceptibility of six sour orange rootstocks. Acta Phytopathol Sinica 9:61–72Google Scholar
  15. FAO (1994) Statistical summary of agricultural production. FAO Quart Bull Stat 7:14Google Scholar
  16. Frost HB (1926) Polyembryony, heterozygosity and chimeras in citrus. Hilgardia 1:365–402Google Scholar
  17. Frost HB, Soost RK (1968) Seed reproduction: development of gametes and embryos. In: Reuther W, Webber HJ, Barchelor LD (eds) The Citrus industry. University of California, Berkeley, pp 290–324Google Scholar
  18. Green RM, Vardi A, Galun E (1986) The plastome of Citrus. Physical map, variation among Citrus cultivars and species and comparison with related genera. Theor Appl Genet 72:170–177Google Scholar
  19. Guerra MS (1984) Cytogenetics of Rutaceae. II. Nuclear DNA content. Caryologia 37:219–226Google Scholar
  20. Guerra MS (1993) Cytogenetics of rutaceae. V. High chromosomal variability in Citrus species revealed by CMA/DAPI staining. Heredity 71:234–241Google Scholar
  21. Hillis DM (1984) Misuse and modification of Nei's distance. Systematic Zool 33:238240Google Scholar
  22. Iwamasa M, Nito N (1988) Cytogenetics and the evolution of modern cultivated citrus. In: Goren R, Mendel K (ed) Proc 6th Int Citrus Cong Margraf Scientific Books, Weikersheim, pp 265–275Google Scholar
  23. Iwamase M, Nito N, Ling JT (1988) Intra- and inter-generic hybridization in the orange subfamily, Aurantioideae Proc Int Soc Citriculture 1:123–130Google Scholar
  24. Khan IA, Roose ML (1988) Frequency and characteristics of nucellar and zygotic seedlings in three cultivars of trifoliate orange. J Am Soc Hort Sci 113:105–110Google Scholar
  25. Moore GA, Castle WS (1988) Morphology and isozymic analysis of open-pollinated citrus rootstock populations. J Hered 79:59–63Google Scholar
  26. Navarro L, Juarez J, Pina JA, Ballester JF, Arregui JM (1988) The citrus variety improvement program in Spain after eleven years. In: Timmer LW, Garnsey SM, Navarro L (eds) Proc 10th Conf Int Organization Citrus Virology. University of California, Riverside, pp 400–406Google Scholar
  27. Ortiz JM (1986) Nomenclatura botánica de los cítricos. Fruits 41:199–209Google Scholar
  28. Patterson C (ed.) (1987) Molecules and morphology in evolution: conflict or compromise? Cambridge University Press, CambridgeGoogle Scholar
  29. Pérez de la Vega M (1993) Biochemical characterization of populations. In: Hayward MD, Bosemark NO, Romagosa I (eds) Plant breeding. Chapman and Hall, Cambridge, pp 184–212Google Scholar
  30. Raghuvanshi SS (1962) Cytological studies in genus Citrus. IV. Evolution in the genus Citrus. Cytologia 27:172–188Google Scholar
  31. Roose ML (1988) Isozyme and DNA restriction fragment length polymorphisms in citrus breeding and systematic. Proc. 6th Int Citrus Cong, pp 155–165Google Scholar
  32. Roose ML, Cheng FS, Federici CT (1994) Origin, inheritance and effects of a dwarfing gene from the citrus rootstock Poncirus trifoliata “Flying Dragon”. HortScience 29:482Google Scholar
  33. Scora RW, Kumamoto J (1983) Chemotaxonomy of the genus Citrus. In: Waterman PG, Grundon MF (eds.) Chemistry and chemical taxonomy of the rutales. Academic Press, London, pp 343–351Google Scholar
  34. Singh R, Nath N (1969) Practical approach to the classification of citrus. Proc 1st Int Citrus Symp 1:435–440Google Scholar
  35. Soost RK (1964) Self-incompatibility in Citrus grandis (Linn.) Osbeck, Proc Am Soc Hort Sci 84:137–140Google Scholar
  36. Swingle WT (1943) The botany of Citrus and its relatives of the orange subfamily. In: Webber HJ, Batchelor LD (eds) The Citrus industry. University of California, BerkeleyGoogle Scholar
  37. Swofford DL, Olsen GJ (1990) Phylogeny reconstruction. In: Hillis DM, Moritz C (eds) Molecular systematics. Sinauer Associates, Massachusetts, pp 411–501Google Scholar
  38. Tanaka T (1969) Misunderstanding with regards citrus classification and nomenclature. Bull Univ Osaka Prefect, Ser B Agric 21:139–145Google Scholar
  39. Torres AM, Soost RK, Diedenhofen U (1978) Leaf isozymes as genetic markers in Citrus. Am J Bot 65:869–881Google Scholar
  40. Torres AM, Soost RK, Mau-Lastovicka T (1982) Citrus isozymes. J Hered 73:335–339Google Scholar
  41. Torres AM, Mau-Lastovicka T, Williams TE, Soost RK (1985) Segregation distortion and linkage of Citrus and Poncirus isozyme genes. J Hered 76:289–294Google Scholar
  42. Van Vuuren SP, Greech NM, Collins RP (1991) Reaction of Gou-Tou orange to citrus nematode, Phytophthora and citrus tristeza virus. In: Brlansky RH, Lee RF, Timmer LW (eds) Proc 11th Conf Int Org Citrus Virology. University of California, Riverside, pp 128–134Google Scholar
  43. Wilson AC, Sarich VM, Maxson LR (1974) The importance of gene arrangements in evolution: evidence from studies of rates of chromosomal, protein and anatomical evolution. Proc Natl Acad Sci USA 71:3028–3030Google Scholar
  44. Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:473–639Google Scholar
  45. Wright S (1978) Evolution and genetics of populations, vol 4. Variability in and among natural populations. University Chicago Press, ChicagoGoogle Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • R. Herrero
    • 1
  • M. J. Asíns
    • 1
  • E. A. Carbonell
    • 1
  • L. Navarro
    • 1
  1. 1.Instituto Valenciano de Investigaciones AgrariasMoncadaSpain

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