Advertisement

Ploidy Manipulation for Citrus Breeding, Genetics, and Genomics

  • Patrick OllitraultEmail author
  • Maria Antonietta Germanà
  • Yann Froelicher
  • Jose Cuenca
  • Pablo Aleza
  • Raphaël Morillon
  • Jude W. Grosser
  • Wenwu Guo
Chapter
Part of the Compendium of Plant Genomes book series (CPG)

Abstract

Polyploidy appears to have played a limited role in citrus germplasm evolution. However, today, ploidy manipulation is an important component of citrus breeding strategies. For varieties, the main objective is to develop triploid seedless cultivars. For rootstock, the aim is to cumulate interesting traits in tetraploid hybrids and to improve adaptation to biotic and abiotic stresses. This chapter starts with a review of the recent knowledge acquired on the natural mechanisms of citrus polyploidization and tetraploid meiosis. Chromosome doubling of nucellar cells is frequent in apomictic citrus and results in tetraploid seedling production. Unreduced gametes are also frequently produced, mainly by second division restitution for ovules. First division restitution was described for pollen as well as alternative mechanisms for both ovules and pollen. Tetraploid plants display tetrasomic to disomic segregations in relation to their genome structure (autotetraploid versus allotetraploid) and the divergence of the parental species. The implications of the origin of diploid gametes, on the genetic diversity of polyploid progenies, are discussed. The biotechnological tools (haplomethods, chromosome doubling by chemical treatments, somatic hybridization, and cytogenetic/molecular tools for polyploid genome studies) used to optimize ploidy manipulation are presented. The interest of haploid and polyploid genotypes for basic genetic and genomic studies is discussed. The research areas reviewed are as follows: haploids and doubled haploids for genome sequencing and haplotyping, centromere mapping from unreduced gametes, marker–trait association study in polyploids, and phenome and gene expression in polyploids with a special focus on polyploidy and adaptation. Finally, we give an overview of the recent advances of concrete polyploid citrus breeding programs in China, Florida, and the Mediterranean Basin.

Keywords

Triploid Tetraploid Haploid Doubled haploid Meiosis 2n gametes Somatic hybridization Molecular markers Adaptation 

References

  1. Adams KL, Percifield R, Wendel JF (2004) Organ-specific silencing of duplicated genes in a newly synthesized cotton allotetraploid. Genetics 168(4):2217–2226.  https://doi.org/10.1534/genetics.104.033522CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ahmed D, Comte A, Curk F et al (2019) A Pipe-line for phylogenomic inference from genotyping by sequencing data in large diploid and polyploid population; an application to Citrus germplasm. Ann BotGoogle Scholar
  3. Aleza P, Juarez J, Hernandez M et al (2009) Recovery and characterization of a Citrus clementina Hort. ex Tan. ‘Clemenules’ haploid plant selected to establish the reference whole Citrus genome sequence. BMC Plant Biol 9:110.  https://doi.org/10.1186/1471-2229-9-110PubMedPubMedCentralCrossRefGoogle Scholar
  4. Aleza P, Juarez J, Ollitrault P et al (2009b) Production of tetraploid plants of non apomictic citrus genotypes. Plant Cell Rep 28(12):1837–1846.  https://doi.org/10.1007/s00299-009-0783-2CrossRefPubMedPubMedCentralGoogle Scholar
  5. Aleza P, Juarez J, Cuenca J et al (2010) Recovery of citrus triploid hybrids by embryo rescue and flow cytometry from 2x × 2x sexual hybridisation and its application to extensive breeding programs. Plant Cell Rep 29(9):1023–1034.  https://doi.org/10.1007/s00299-010-0888-7CrossRefPubMedPubMedCentralGoogle Scholar
  6. Aleza P, Froelicher Y, Schwarz S et al (2011) Tetraploidization events by chromosome doubling of nucellar cells are frequent in apomictic citrus and are dependent on genotype and environment. Ann Bot 108(1):37–50.  https://doi.org/10.1093/aob/mcr099CrossRefPubMedPubMedCentralGoogle Scholar
  7. Aleza P, Juarez J, Hernndez M et al (2012a) Implementation of extensive citrus triploid breeding programs based on 4x × 2x sexual hybridisations. Tree Genet Genom 8(6):1293–1306.  https://doi.org/10.1007/s11295-012-0515-6CrossRefGoogle Scholar
  8. Aleza P, Juarez J, Cuenca J et al (2012b) Extensive citrus triploid hybrid production by 2x×4x sexual hybridizations and parent-effect on the length of the juvenile phase. Plant Cell Rep 31(9):1723–1735.  https://doi.org/10.1007/s00299-012-1286-0;10.1007/s00299-012-1286-0CrossRefPubMedPubMedCentralGoogle Scholar
  9. Aleza P, Cuenca J, Hernandez M et al (2015) Genetic mapping of centromeres in the nine Citrus clementina chromosomes using half-tetrad analysis and recombination patterns in unreduced and haploid gametes. BMC Plant Biol 15:80.  https://doi.org/10.1186/s12870-015-0464-yPubMedPubMedCentralCrossRefGoogle Scholar
  10. Aleza P, Cuenca J, Juarez J et al (2016) Inheritance in doubled-diploid clementine and comparative study with SDR unreduced gametes of diploid clementine. Plant Cell Rep 35(8):1573–1586.  https://doi.org/10.1007/s00299-016-1972-4PubMedCrossRefPubMedCentralGoogle Scholar
  11. Allario T, Brumos J, Colmenero-Flores JM et al (2011) Large changes in anatomy and physiology between diploid Rangpur lime (Citrus limonia) and its autotetraploid are not associated with large changes in leaf gene expression. J Exp Bot 62(8):2507–2519.  https://doi.org/10.1093/jxb/erq467PubMedCrossRefPubMedCentralGoogle Scholar
  12. Allario T, Brumos J, Colmenero-Flores JM et al (2013) Tetraploid Rangpur lime rootstock increases drought tolerance via enhanced constitutive root abscisic acid production. Plant Cell Environ 36(4):856–868.  https://doi.org/10.1111/pce.12021CrossRefGoogle Scholar
  13. Atanassov A, Zagorska N, Boyadjiev P et al (1995) In vitro production of haploid plants. World J Microbiol Biotechnol 11:400–408.  https://doi.org/10.1007/BF00364615CrossRefPubMedPubMedCentralGoogle Scholar
  14. Balal RM, Shahid MA, Vincent C et al (2017) Kinnow mandarin plants grafted on tetraploid rootstocks are more tolerant to Cr-toxicity than those grafted on its diploids one. Environ Exp Bot 140:8–18.  https://doi.org/10.1016/j.envexpbot.2017.05.011CrossRefGoogle Scholar
  15. Banuls J, Serna MD, Legaz F et al (1997) Growth and gas exchange parameters of Citrus plants stressed with different salts. J Plant Physiol 150(1):194–199.  https://doi.org/10.1016/S0176-1617(97)80202-7CrossRefGoogle Scholar
  16. Barone A, Gebhardt C, Frusciante L (1995) Heterozygosity in 2n gametes of potato evaluated by RFLP markers. Theor Appl Genet 91(1):98–104.  https://doi.org/10.1007/BF00220864CrossRefPubMedPubMedCentralGoogle Scholar
  17. Barrett HC (1974) Colchicine-induced polyploidy in Citrus. Botanical Gazette 135.  https://doi.org/10.1086/336726CrossRefGoogle Scholar
  18. Barrett HC, Hutchison DJ (1978) Spontaneous tetraploidy in apomictic seedlings ofCitrus. Econ Bot 32(1):27–45.  https://doi.org/10.1007/BF02906727CrossRefGoogle Scholar
  19. Bassene JB, Berti L, Costantino G et al (2009a) Inheritance of characters involved in fruit quality in a citrus interspecific allotetraploid somatic hybrid. J Agric Food Chem 57(11):5065–5070.  https://doi.org/10.1021/jf803872fCrossRefPubMedPubMedCentralGoogle Scholar
  20. Bassene JB, Froelicher Y, Dhuique-Mayer C et al (2009) Non-additive phenotypic and transcriptomic inheritance in a citrus allotetraploid somatic hybrid between C. reticulata and C. limon: the case of pulp carotenoid biosynthesis pathway. Plant Cell Rep 28(11):1689–1697.  https://doi.org/10.1007/s00299-009-0768-1PubMedCrossRefPubMedCentralGoogle Scholar
  21. Bassene JB, Froelicher Y, Dubois C et al (2010) Non-additive gene regulation in a citrus allotetraploid somatic hybrid between C. reticulata Blanco and C. limon (L.) Burm. Heredity 105(3):299–308.  https://doi.org/10.1038/hdy.2009.162PubMedCrossRefPubMedCentralGoogle Scholar
  22. Beloti VH, Alves G, Coletta-Filho H et al (2018) The Asian citrus psyllid host Murraya koenigii is immune to citrus Huanglongbing pathogen Candidatus Liberibacter asiaticus. Phytopathology.  https://doi.org/10.1094/PHYTO-01-18-0012-RCrossRefPubMedPubMedCentralGoogle Scholar
  23. Bottani S, Zabet NR, Wendel JF et al (2018) Gene expression dominance in allopolyploids: hypotheses and models. Trends Plant Sci 23(5):393–402.  https://doi.org/10.1016/j.tplants.2018.01.002CrossRefPubMedPubMedCentralGoogle Scholar
  24. Bretagnolle F, Thompson JD (1995) Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol 129(1):1–22.  https://doi.org/10.1111/j.1469-8137.1995.tb03005.xCrossRefGoogle Scholar
  25. Cabasson C, Ollitrault P, Côte F et al (1995) Characteristics of Citrus cell cultures during undifferentiated growth on sucrose and somatic embryogenesis on galactose. Physiol Plantarum 93(3):464–470.  https://doi.org/10.1111/j.1399-3054.1995.tb06844.xCrossRefGoogle Scholar
  26. Cameron J, Frost H (1968) Genetics, breeding and nucellar embryony. In: Reuther LB, Webber H (eds) The citrus industry, vol II. Univ. Calif. Press, Berkeley, pp 325–370Google Scholar
  27. Cameron JW, Soost RK (1970) Characters of new populations of Citrus polyploids, and the relation between tetraploidy in the pollen parent and hybrid tetraploid progeny. In: Proceedings of the 1st international citrus symposium, vol 1, pp 199–205Google Scholar
  28. Cao H, Biswas MK, Lu Y et al (2011) Doubled haploid callus lines of Valencia sweet orange recovered from anther culture. Plant Cell Tiss Org Cult 104(3):415–423.  https://doi.org/10.1007/s11240-010-9860-zCrossRefGoogle Scholar
  29. Cardoso J, Martinelli A, Germanà MA et al (2014) In vitro anther culture of sweet orange (Citrus sinensis L. Osbeck) genotypes and of a C. clementina × C. sinensis Hamlin hybrid. Plant Cell, Tissue Organ Cult 117:455–464.  https://doi.org/10.1007/s11240-014-0456-xCrossRefGoogle Scholar
  30. Cardoso J, Mohamed Abdelgalel A, Chiancone B et al (2015) Gametic and somatic embryogenesis through in vitro anther culture of different Citrus genotypes. Plant Biosystems 150:1–9.  https://doi.org/10.1080/11263504.2014.987847CrossRefGoogle Scholar
  31. Chen ZJ (2010) Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci 15(2):57–71.  https://doi.org/10.1016/j.tplants.2009.12.003CrossRefPubMedPubMedCentralGoogle Scholar
  32. Chen Z, Wang H, Liao H (1980) The induction of Citrus pollen plants in artificial media. Acta Genetica Sinica 7:189–192Google Scholar
  33. Chiancone B, Germanà MA (2016) Microspore embryogenesis through anther culture in Citrus clementina Hort. ex Tan. In: Germanà MA, Lambardi M (eds) In vitro embryogenesis in higher plants. New York, NY, Springer, New York, pp 475–487CrossRefGoogle Scholar
  34. Chiancone B, Tassoni A, Bagni N et al (2006) Effect of polyamines on in vitro anther culture of Citrus clementina Hort. ex Tan. Plant Cell, Tissue Organ Cult 87(2):145–153.  https://doi.org/10.1007/s11240-006-9149-4CrossRefGoogle Scholar
  35. Chiancone B, Karasawa MMG, Gianguzzi V et al (2015) Early embryo achievement through isolated microspore culture in Citrus clementina Hort. ex Tan., cvs. Monreal Rosso and Nules. Front Plant Sci 6:413.  https://doi.org/10.3389/fpls.2015.00413
  36. Chu C-, Xu SS, Friesen TL et al (2008) Whole genome mapping in a wheat doubled haploid population using SSRs and TRAPs and the identification of QTL for agronomic traits. Mol Breed 22(2):251–266.  https://doi.org/10.1007/s11032-008-9171-9CrossRefGoogle Scholar
  37. Cimò G,  Casamento D, Torello Marinoni D e al. (2016) Gametic embryogenesis through isolated microspore culture in mandarin (Citrus reticulata Blanco), cv Mandarino Tardivo Di Ciaculli: effect of meta-topolin and temperature treatments. Citrus Res Technol 37(2):113–122CrossRefGoogle Scholar
  38. Comai L, Tyagi AP, Winter K et al (2000) Phenotypic instability and rapid gene silencing in newly formed arabidopsis allotetraploids. Plant Cell 12(9):1551–1568PubMedPubMedCentralCrossRefGoogle Scholar
  39. Crespel L, Gudin S (2003) Evidence for the production of unreduced gametes by tetraploid Rosa hybrida L. Euphytica 133:65–69.  https://doi.org/10.1023/A:1025640405827CrossRefGoogle Scholar
  40. Cuenca J, Aleza P, Juárez J et al (2010) ‘Safor’ mandarin: a new citrus mid-late triploid hybrid. HortScience 45(6):977–980CrossRefGoogle Scholar
  41. Cuenca J, Froelicher Y, Aleza P et al (2011) Multilocus half-tetrad analysis and centromere mapping in citrus: evidence of SDR mechanism for 2n megagametophyte production and partial chiasma interference in mandarin cv ‘Fortune’. Heredity (Edinb) 107(5):462–470.  https://doi.org/10.1038/hdy.2011.33PubMedPubMedCentralCrossRefGoogle Scholar
  42. Cuenca J, Aleza P, Navarro L et al (2013a) Assignment of SNP allelic configuration in polyploids using competitive allele-specific PCR: application to citrus triploid progeny. Ann Bot 111(4):731–742.  https://doi.org/10.1093/aob/mct032PubMedPubMedCentralCrossRefGoogle Scholar
  43. Cuenca J, Aleza P, Vicent A et al (2013b) Genetically based location from triploid populations and gene ontology of a 3.3-mb genome region linked to alternaria brown spot resistance in citrus reveal clusters of resistance genes. PLoS One 8(10):e76755.  https://doi.org/10.1371/journal.pone.0076755PubMedPubMedCentralCrossRefGoogle Scholar
  44. Cuenca J, Aleza P, Juarez J et al (2015) Maximum-likelihood method identifies meiotic restitution mechanism from heterozygosity transmission of centromeric loci: application in citrus. Sci Rep 5:9897.  https://doi.org/10.1038/srep09897
  45. Curk F, Ancillo G, Ollitrault F et al (2015) Nuclear species-diagnostic SNP markers mined from 454 amplicon sequencing reveal admixture genomic structure of modern citrus varieties. PLoS One 10(5):e0125628.  https://doi.org/10.1371/journal.pone.0125628PubMedPubMedCentralCrossRefGoogle Scholar
  46. Curtolo M, Cristofani-Yaly M, Gazaffi R et al (2017) QTL mapping for fruit quality in Citrus using DArTseq markers. BMC Genom 18(1):289.  https://doi.org/10.1186/s12864-017-3629-2
  47. Daccord N, Celton J, Linsmith G et al (2017) High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet 49:1099PubMedCrossRefPubMedCentralGoogle Scholar
  48. Dalkilic Z, Timmer LW, Gmitter FG Jr (2005) Linkage of an alternaria disease resistance gene in Mandarin hybrids with RAPD fragments. J Am Soc Hort Sci 130(2):191–195CrossRefGoogle Scholar
  49. Dambier D, Benyahia H, Pensabene-Bellavia G et al (2011) Somatic hybridization for citrus rootstock breeding: an effective tool to solve some important issues of the Mediterranean citrus industry. Plant Cell Rep 30(5):883–900.  https://doi.org/10.1007/s00299-010-1000-zPubMedCrossRefGoogle Scholar
  50. Datta SK (2005) Androgenic haploids: Factors controlling development and its application in crop improvement. Curr Sci 89(11):1870–1878Google Scholar
  51. De Jong W, De Jong D, Bodis M (2003) A fluorogenic 5’ nuclease (TaqMan) assay to assess dosage of a marker tightly linked to red skin color in autotetraploid potato. Theor Appl Genet 107:1384–1390.  https://doi.org/10.1007/s00122-003-1420-zCrossRefPubMedPubMedCentralGoogle Scholar
  52. De Storme N, Geelen D (2013) Sexual polyploidization in plants cytological mechanisms and molecular regulation. New Phytol 198(3):670–684.  https://doi.org/10.1111/nph.12184CrossRefPubMedPubMedCentralGoogle Scholar
  53. Deng XX, Deng ZA, Xiao SY et al (1992) Pollen derived plantlets from anther culture of Ichang papeda hybrids No. 14 and Trifoliate orange. In: Anonymous proceedings of the international society Citriculture. Acireale, Italy, pp 190–192Google Scholar
  54. Deng XX, Grosser JW, Gmitter FG (1992) Fertility of somatic hybrids between Citrus aurantifolia and C. sinensis. [Chinese]. Hereditas (Beijing) 14(1):8–9Google Scholar
  55. Dewitte A, Huylenbroeck JV, Laere KV (2012) Use of 2n gametes in plant breeding. In: Abdurakhmonov I (ed) Plant breeding. InTech, RijekaGoogle Scholar
  56. D’Hont A, Denoeud F, Aury J et al (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213PubMedCrossRefPubMedCentralGoogle Scholar
  57. Douches D, Maas D,L. (1998) Comparison of FDR- and SDR-derived tetraploid progeny from 2x × 4x crosses using haploids of Solanum tuberosum L. that produce mixed modes of 2n eggs. Theor Appl Genet 97:1307–1313.  https://doi.org/10.1007/s001220051023CrossRefGoogle Scholar
  58. Douches DS, Quiros CF (1987) Use of 4x × 2x crosses to determine gene-centromere map distances of isozyme loci in Solanum species. Genome 29(4):519–527.  https://doi.org/10.1139/g87-089CrossRefGoogle Scholar
  59. Dutra de Souza J, de Andrade Silva E, Coelho Filho MA et al (2017) Different adaptation strategies of two citrus scion/rootstock combinations in response to drought stress. PLoS ONE 12(5):e0177993PubMedPubMedCentralCrossRefGoogle Scholar
  60. Eck Y, Moragues M, Ferrante S et al (2016) Development and application of affymetrix SNP arrays for citrus. Book of Abstract; Sustainable Citriculture. The role of applied knowledge International Citrus CongressGoogle Scholar
  61. Esen A, Soost RK (1971) Unexpected triploids in citrus: their origin, identification and possible use. J Heredity 62:329–333CrossRefGoogle Scholar
  62. Esen A, Soost RK (1973) Precocious development and germination of spontaneous triploid seeds in Citrus. J Hered 64(3):147–154CrossRefGoogle Scholar
  63. Esen A, Soost RK, Geraci G (1979) Genetic evidence for the origin of diploid megagametophytes in Citrus. J Hered 70.  https://doi.org/10.1093/oxfordjournals.jhered.a109188CrossRefGoogle Scholar
  64. Esselink G, Nybom H, Vosman B (2004) Assignment of allelic configuration in polyploids using the MAC-PR (microsatellite DNA allele counting—peak ratios) method. Theor Appl Genet 109(2):402–408PubMedCrossRefPubMedCentralGoogle Scholar
  65. Ferrante SP, Lucretti S, Reale S et al (2010) Assessment of the origin of new citrus tetraploid hybrids (2n = 4x) by means of SSR markers and PCR based dosage effects. Euphytica 173(2):223–233CrossRefGoogle Scholar
  66. Flagel LE, Wendel JF (2010) Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytol 186(1):184–193.  https://doi.org/10.1111/j.1469-8137.2009.03107.xCrossRefPubMedPubMedCentralGoogle Scholar
  67. Flagel L, Udall J, Nettleton D et al (2008) Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biol 6(1):16PubMedPubMedCentralCrossRefGoogle Scholar
  68. Froelicher Y, Ollitrault P (2000) Effects of the hormonal balance on Clausena excavata androgenesis. Acta Horticulturae 535:139–146Google Scholar
  69. Froelicher Y, Luro F, Ollitrault P (2000) Analysis of meiotic behavior of the tetraploid Clausena excavata species by molecular marker segregation studies. In: Anonymous international society of citriculture congress 2000. Program and abstracts, Orlando edn. International Society of citriculture, OrlandoGoogle Scholar
  70. Froelicher Y, Bassene JB, Jedidi-Neji E et al (2007) Induced parthenogenesis in mandarin for haploid production: induction procedures and genetic analysis of plantlets. Plant Cell Rep 26(7):937–944.  https://doi.org/10.1007/s00299-007-0314-yPubMedCrossRefPubMedCentralGoogle Scholar
  71. Fujii H, Shimada T, Nonaka K et al (2013) High-throughput genotyping in citrus accessions using an SNP genotyping array. Tree Genet Genom 9(1):145–153.  https://doi.org/10.1007/s11295-012-0542-3CrossRefGoogle Scholar
  72. Gancel AL, Ollitrault P, Froelicher Y et al (2003) Leaf volatile compounds of seven citrus somatic tetraploid hybrids sharing willow leaf mandarin (Citrus deliciosa Ten.) as their common parent. J Agric Food Chem 51(20):6006–6013.  https://doi.org/10.1021/jf0345090PubMedCrossRefPubMedCentralGoogle Scholar
  73. Gancel AL, Grimplet J, Sauvage FX et al (2006) Predominant expression of diploid mandarin leaf proteome in two citrus mandarin-derived somatic allotetraploid hybrids. J Agric Food Chem 54(17):6212–6218.  https://doi.org/10.1021/jf060657pCrossRefPubMedPubMedCentralGoogle Scholar
  74. Garcia-Lor A, Ancillo G, Navarro L et al (2013) Citrus (Rutaceae) SNP markers based on competitive allele-specific PCR; transferability across the Aurantioideae subfamily. Appl Plant Sci 1(4).  https://doi.org/10.3732/apps.1200406CrossRefGoogle Scholar
  75. Garcia-Lor A, Curk F, Snoussi-Trifa H et al (2013) A nuclear phylogenetic analysis: SNPs, indels and SSRs deliver new insights into the relationships in the ‘true citrus fruit trees’ group (Citrinae, Rutaceae) and the origin of cultivated species. Ann Bot 111(1):1–19.  https://doi.org/10.1093/aob/mcs227PubMedPubMedCentralCrossRefGoogle Scholar
  76. Geraci G, Esen A, Soost RK (1975) Triploid progenies of Citrus cultivars from 2x × 2x crosses. J Hered 66(3):177–178.  https://doi.org/10.1093/oxfordjournals.jhered.a108607CrossRefGoogle Scholar
  77. Germanà MA (2003) Haploids and doubled haploids in Citrus ssp. In: Maluszynski M, Kasha KJ, Forster BP et al (eds) Doubled haploid production in crop plants: a manual. Springer, Netherlands, Dordrecht, pp 303–307CrossRefGoogle Scholar
  78. Germanà MA (2006) Doubled haploid production in fruit crops. Plant Cell Tiss Org Cult 86:131–146.  https://doi.org/10.1007/s11240-006-9088-0CrossRefGoogle Scholar
  79. Germanà MA (2007) Haploidy. In: Khan IA (ed) Citrus. Genetics, breeding and biotechnology. CABI, pp 167–196Google Scholar
  80. Germanà MA (2009) Haploids and doubled haploids in fruit trees. In: Touraev A, Forster BP, Jain SM (eds) Advances in haploid production in higher plants. Springer, Netherlands, Dordrecht, pp 241–263CrossRefGoogle Scholar
  81. Germanà MA (2011a) Gametic embryogenesis and haploid technology as valuable support to plant breeding. Plant Cell Rep 30(5):839–857.  https://doi.org/10.1007/s00299-011-1061-7CrossRefPubMedPubMedCentralGoogle Scholar
  82. Germanà MA (2011b) Anther culture for haploid and doubled haploid production. Plant Cell, Tissue Organ Cult 104:283–300.  https://doi.org/10.1007/s11240-010-9852-zCrossRefGoogle Scholar
  83. Germanà MA (2012) Use of irradiated pollen to induce parthenogenesis and haploid production in fruit crops. Plant Mutat Breed Biotechnol:411–421Google Scholar
  84. Germanà MA (2017) Microspore embryogenesis in Citrus and other fruit crops. Acta Hortic. 1187. International Society for Horticultural Science (ISHS), Leuven, Belgium, p 139-155Google Scholar
  85. Germanà MA, Chiancone B (2001) Gynogenetic haploids of Citrus after in vitro pollination with triploid pollen grains. Plant Cell Tissue Organ Cult 66(1):59–66.  https://doi.org/10.1023/A:1010627310808CrossRefGoogle Scholar
  86. Germanà MA, Chiancone B (2003) Improvement of Citrus clementina Hort. ex Tan. microspore-derived embryoid induction and regeneration. Plant Cell Rep 22(3):181–187.  https://doi.org/10.1007/s00299-003-0669-7
  87. Germanà MA, Reforgiato Recupero G (1997) Haploid embryos regeneration from anther culture of ‘Mapo’ tangelo (Citrus deliciosa × C. paradisi). Adv Hortic Sci 11(3):147–152Google Scholar
  88. Germanà MA, Crescimanno FG, De Pasquale F et al (1992) Androgenesis in 5 cultivars of Citrus limon L. Burm. F. Acta Horticulturae 300:315–324.  https://doi.org/10.17660/actahortic.1992.300.46
  89. Germanà MA, Ying Wang Y, Barbagallo MG et al (1994) Recovery of haploid and diploid plantlets from anther culture of Citrus clementina Hort, ex Tan. and Citrus reticulata Blanco. J Hortic Sci 69(3):473–480.  https://doi.org/10.1080/14620316.1994.11516478CrossRefGoogle Scholar
  90. Germanà MA, Scarano MT, Crescimanno FG (1996) First results on isolated microspore culture of Citrus. Proc Int Soc Citricult 2:882–885Google Scholar
  91. Germanà MA, Crescimanno FG, Reforgiato Recupero G et al (2000a) Preliminary characterization of several doubled haploids of Citrus clementina cv. Nules. Acta Horticulturae 535:183–190CrossRefGoogle Scholar
  92. Germanà MA, Crescimanno FG, Motisi A (2000b) Factors affecting androgenesis in Citrus clementina Hort. ex Tan. Adv Hortic Sci 14:43–51Google Scholar
  93. Germanà MA, Chiancone B, Lain O et al (2005) Anther culture in Citrus clementina: a way to regenerate tri-haploids. AUST J AGR RES 56:839–845.  https://doi.org/10.1071/AR05025CrossRefGoogle Scholar
  94. Germanà MA, Aleza P, Carrera E et al (2013) Cytological and molecular characterization of three gametoclones of Citrus clementina. BMC Plant Biol 13:129.  https://doi.org/10.1186/1471-2229-13-129
  95. Gmitter FG Jr, Ling XB (1991) Embryogenesis in vitro and nonchimeric tetraploid plant recovery from undeveloped Citrus ovules treated with colchicine. J Am Soc Hort Sci 116(2):317–321CrossRefGoogle Scholar
  96. Gmitter FG Jr, Ling XB, Cai CY et al (1991) Colchicine-induced polyploidy in Citrus embryogenic cultures, somatic embryos, and regenerated plantlets. Plant Sci (Limerick) 74(1):135–141CrossRefGoogle Scholar
  97. Grant V (1981) Plant speciation, 2nd edn. Colombia University Press, New YorkCrossRefGoogle Scholar
  98. Grosser JW, Gmitter FG Jr (1990) Protoplast fusion and citrus improvement. Plant Breed Rev 8:339–374Google Scholar
  99. Grosser JW, Gmitter FG (2011) Protoplast fusion for production of tetraploids and triploids: applications for scion and rootstock breeding in citrus. (Special Issue: In vitro ploidy manipulation in the genomics era.). Plant Cell, Tissue Organ Cult 104(3):343–357Google Scholar
  100. Grosser JW, Gmitter FG Jr, Tusa N et al (1990) Somatic hybrid plants from sexually incompatible woody species: Citrus reticulata and Citropsis gilletiana. Plant Cell Rep 8(11):656–659PubMedCrossRefPubMedCentralGoogle Scholar
  101. Grosser JW, Gmitter FG Jr, Sesto F et al (1992) Six new somatic citrus hybrids and their potential for cultivar improvement. J Am Soc Hort Sci 117(1):169–173CrossRefGoogle Scholar
  102. Grosser JW, Gmitter FG, Chandler JL et al (1994) Somatic hybridization of complementary citrus rootstock: five new hybrids. HortScience 29(7):812–813CrossRefGoogle Scholar
  103. Grosser JW, MouraoFo FAA, Gmitter FG Jr et al (1996) Allotetraploid hybrids between Citrus and seven related genera produced by somatic hybridization. Theor Appl Genet 92(5):577–582PubMedCrossRefPubMedCentralGoogle Scholar
  104. Grosser JW, Ollitrault P, OlivaresFuster O (2000) Somatic hybridization in citrus: an effective tool to facilitate variety improvement. Vitro Cell Dev Biol Plant 36(6):434–449CrossRefGoogle Scholar
  105. Grosser JW, Graham JH, McCoy CW et al (2003) Development of “tetrazyg” rootstocks tolerant of the diaprepes/phytophthora complex under greenhouse conditions. Proc Fla State Hort Soc 116:262–267Google Scholar
  106. Grosser JW, Chandler JL, Duncan LW (2007) Production of mandarin + pummelo somatic hybrid citrus rootstocks with potential for improved tolerance/resistance to sting nematode. Sci Hortic 113(1):33–36CrossRefGoogle Scholar
  107. Grosser JW, Calovic M, Louzada E (2010) Protoplast fusion technology: somatic hybridization and cybridization. In: Davey MR, Anthony P (eds) Plant cell culture: essential methods. Wiley Online Library, pp 175–198Google Scholar
  108. Grosser JW, HyunJoo An, Calovic M et al (2010b) Production of new allotetraploid and autotetraploid citrus breeding parents: focus on zipperskin mandarins. HortScience 45(8):1160–1163CrossRefGoogle Scholar
  109. Grosser JW, Kainth D, Dutt M (2014) Production of colchicine-induced autotetraploids in pummelo (Citrus grandis Osbeck) through indirect organogenesis. HortScience 49(7):944–948CrossRefGoogle Scholar
  110. Gulsen O, Uzun A, Canan I et al (2010) A new citrus linkage map based on SRAP, SSR, ISSR, POGP, RGA and RAPD markers. Euphytica 173(2):265–277CrossRefGoogle Scholar
  111. Guo WW, Deng XX (1999) Intertribal hexaploid somatic hybrid plants regeneration from electrofusion between diploids of Citrus sinensis and its sexually incompatible relative, Clausena lansium. Theor Appl Genet 98(3):581–585.  https://doi.org/10.1007/s001220051107CrossRefGoogle Scholar
  112. Guo WW, Deng XX (2001) Wide somatic hybrids of Citrus with its related genera and their potential in genetic improvement. Euphytica 118(2):175–183.  https://doi.org/10.1023/A:1004147208099CrossRefGoogle Scholar
  113. Guo W-, Deng X, Shi Y- (1998) Optimization of electrofusion parameters and interspecific somatic hybrids regeneration in Citrus. Acta Bot Sinica 40:417–424Google Scholar
  114. Guo WW, Wu RC, Cheng YJ et al (2007) Production and molecular characterization of Citrus intergeneric somatic hybrids between red tangerine and citrange. Plant Breed 126:72–76.  https://doi.org/10.1111/j.1439-0523.2006.01315.xCrossRefGoogle Scholar
  115. Guo W, Xiao S, Deng X (2013) Somatic cybrid production via protoplast fusion for citrus improvement. Sci Hortic 163:20–26.  https://doi.org/10.1016/j.scienta.2013.07.018CrossRefGoogle Scholar
  116. Guo W, Liang W, Xie K et al (2016) Exploitation of polyploids from 39 citrus seedling populations. Acta Hort 1135:11–16CrossRefGoogle Scholar
  117. Harlan JR, deWet JMJ (1975) On winge and a prayer: the origins of polyploidy. Bot Rev 41(4):361–390.  https://doi.org/10.1007/BF02860830CrossRefGoogle Scholar
  118. He P, Friebe BR, Gill BS et al (2003) Allopolyploidy alters gene expression in the highly stable hexaploid wheat. Plant Mol Biol 52:401–414PubMedCrossRefPubMedCentralGoogle Scholar
  119. Hegarty MJ, Barker GL, Wilson ID et al (2006) Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Curr Biol 16:1652–1659PubMedCrossRefPubMedCentralGoogle Scholar
  120. Hidaka T, Yamada Y, Shichijo T (1979) In vitro differentiation of haploid plants by anther culture in Poncirus trifoliata (L.) RAF. Japan J Breed 29(3):248–254.  https://doi.org/10.1270/jsbbs1951.29.248CrossRefGoogle Scholar
  121. Huang S, Kang M, Xu A (2017) HaploMerger2: rebuilding both haploid sub-assemblies from high-heterozygosity diploid genome assembly. Bioinformatics 33(16):2577–2579.  https://doi.org/10.1093/bioinformatics/btx220CrossRefPubMedPubMedCentralGoogle Scholar
  122. Hussain S, Luro F, Costantino G et al (2012) Physiological analysis of salt stress behaviour of citrus species and genera: low chloride accumulation as an indicator of salt tolerance. S Afr J Bot 81:103–112CrossRefGoogle Scholar
  123. Iwamasa M, Nito N (1988) Cytogenetics and the evolution of modern cultivated citrus. In: Anonymous proceeding of the 6th international citrus congress, Tel Aviv, Israel, vol 1. Margraf, Israel, p 265Google Scholar
  124. Iwasaki T (1943) On the big and small leaf strain of trifoliate orange (Poncirus trifoliata Raf.). J Hortic Assoc Jpn 14:302–305CrossRefGoogle Scholar
  125. Iwasaki Y, Nishiki I, Nakamura Y et al (2016) Effective de novo assembly of fish genome using haploid larvae. Gene 576(2):644–649.  https://doi.org/10.1016/j.gene.2015.10.015PubMedCrossRefPubMedCentralGoogle Scholar
  126. Jackson RC, Jackson JW (1996) Gene segregation in autotetraploids: prediction from meiotic configurations. Am J Bot 83(6):673–678.  https://doi.org/10.1002/j.1537-2197.1996.tb12756.xCrossRefGoogle Scholar
  127. Jackson LK, Sherman WB (1975) Chromosome counts in ‘Tahiti’ lime. Florida State Hortic Soc:458–459Google Scholar
  128. Jaskani M, Saghir-ul-Hasnain M, Bashir M et al (1996) Morphological description of citrus colchiploids. In: Proceedings of 8th International Citrus Congress, vol 1, pp 130–132Google Scholar
  129. Jeridi M, Perrier X, Rodier-Goud M et al (2012) Cytogenetic evidence of mixed disomic and polysomic inheritance in an allotetraploid (AABB) Musa genotype. Ann Bot 110(8):1593–1606.  https://doi.org/10.1093/aob/mcs220CrossRefPubMedPubMedCentralGoogle Scholar
  130. Kainth D, Grosser J (2010) Induction of autotetraploids in pummelo (Citrus grandis L. Osbeck) through colchicine treatment of meristematically active seeds in vitro. Proc Fla State Hort Soc 123:44–48Google Scholar
  131. Kamiri M, Stift M, Srairi I et al (2011) Evidence for non-disomic inheritance in a Citrus interspecific tetraploid somatic hybrid between C. reticulata and C. limon using SSR markers and cytogenetic analysis. Plant Cell Rep 30(8):1415–1425.  https://doi.org/10.1007/s00299-011-1050-xPubMedCrossRefPubMedCentralGoogle Scholar
  132. Kauffman EJ, Gestl EE, Kim DJ et al (1995) Microsatellite centromere mapping in the zebrafish (Danio rerio). Genomics 30(2):337–341.  https://doi.org/10.1006/geno.1995.9869CrossRefPubMedPubMedCentralGoogle Scholar
  133. Kobayashi S, Uchimiya H, Ikeda I (1983) Plant Regeneration from ‘Trovita’ Orange Protoplasts. Japan J Breed 33(2):119–122.  https://doi.org/10.1270/jsbbs1951.33.119CrossRefGoogle Scholar
  134. Kobayashi S, Ohgawara T, Saito W et al (1997) Production of triploid somatic hybrids in citrus. J Jpn Soc Hort Sci 66:453–458CrossRefGoogle Scholar
  135. Kochba J, Spiegel-Roy P (1977) Cell and tissue culture for breeding and developmental studies of Citrus. HortScience 12:110–114Google Scholar
  136. Krug CA (1943) Chromosome numbers in the subfamily Arantioideae, with special reference in the genus Citrus. Citrus Bot Gaz 104:602–611CrossRefGoogle Scholar
  137. Landergott U, Naciri Y, Schneller J et al (2006) Allelic configuration and polysomic inheritance of highly variable microsatellites in tetraploid gynodioecious Thymus praecox. Theor Appl Genet 113:453–465.  https://doi.org/10.1007/s00122-006-0310-6CrossRefPubMedPubMedCentralGoogle Scholar
  138. Lapin W (1937) Investigation on polyploidy in Citrus. USSR All Union Scientific Research Institute, vol 1, pp 1–68Google Scholar
  139. Li A, Geng S, Zhang L et al (2015) Making the bread: insights from newly synthesized allohexaploid wheat. Mol Plant 8(6):847–859.  https://doi.org/10.1016/j.molp.2015.02.016CrossRefPubMedPubMedCentralGoogle Scholar
  140. Lim K, Shen T, Barba-Gonzalez R et al (2004) Occurrence of SDR 2N-gametes in Lilium Hybrids. Breed Sci 54(1):13–18.  https://doi.org/10.1270/jsbbs.54.13CrossRefGoogle Scholar
  141. Longley A (1925) Polycarpy, polyspory and polyploidy in Citrus and Citrus relatives. J Wash Acad Sci 15:347–357Google Scholar
  142. Marsden JE, Schwager SJ, May B (1987) Single-locus inheritance in the tetraploid treefrog hyla versicolor with an analysis of expected progeny ratios in tetraploid organisms. Genetics 116(2):299–311PubMedPubMedCentralGoogle Scholar
  143. Martins F, Carneiro P, Guimaraes C et al (2009) Distinction between plant samples according to allele dosage by semiquantitative polymerase chain reaction. Genet Mol Res 8(1):319–327PubMedCrossRefPubMedCentralGoogle Scholar
  144. Mendes BMJ, Filho FdAAM, Farias PCDM et al (2001) Citrus somatic hybridization with potential for improved blight and CTV resistance. Vitro Cell Dev Biol Plant 37(4):490–495.  https://doi.org/10.1007/s11627-001-0086-yCrossRefGoogle Scholar
  145. Mendiburu AO, Peloquin SJ (1979) Gene-centromere mapping by 4x-2x matings in potatoes. Theor Appl Genet 54(4):177–180.  https://doi.org/10.1007/BF00263048CrossRefPubMedPubMedCentralGoogle Scholar
  146. Motomura T, Hidaka T, Monguchi T et al (1995) Intergeneric somatic hybrids between Citrus and Atalantia or Severinia by electrofusion, and recombination of mitochondrial genomes. Japan J Breed 45(3):309–314.  https://doi.org/10.1270/jsbbs1951.45.309CrossRefGoogle Scholar
  147. Mouhaya W, Allario T, Brumos J et al (2010) Sensitivity to high salinity in tetraploid citrus seedlings increases with water availability and correlates with expression of candidate genes. (Special Issue: Improving adaptation to saline environments.). Funct Plant Biol 37(7):674–685Google Scholar
  148. Moya JL, Gómez-Cadenas A, Primo-Millo E et al (2003) Chloride absorption in salt-sensitive Carrizo citrange and salt-tolerant Cleopatra mandarin citrus rootstocks is linked to water use. J Exp Bot 54(383):825–833PubMedCrossRefPubMedCentralGoogle Scholar
  149. Navarro L, Aleza P, Cuenca J et al (2015) The mandarin triploid breeding program in Spain. Acta Hort 1065:389–396CrossRefGoogle Scholar
  150. Nie H, Li Q, Kong L (2012) Centromere mapping in the Pacific abalone (Haliotis discus hannai) through half-tetrad analysis in gynogenetic diploid families. Anim Genet 43(3):290–297.  https://doi.org/10.1111/j.1365-2052.2011.02254.xCrossRefPubMedPubMedCentralGoogle Scholar
  151. Ohgawara T, Kobayashi S, Ohgawara E et al (1985) Somatic hybrid plants obtained by protoplast fusion between Citrus sinensis and Poncirus trifoliata. Theor Appl Genet 71(1):1–4.  https://doi.org/10.1007/BF00278245CrossRefPubMedPubMedCentralGoogle Scholar
  152. Oiyama I, Kobayashi S (1993) Haploids obtained from diploid x triploid crosses of Citrus. J Japan Soc Hortic Sci 62:89–93CrossRefGoogle Scholar
  153. Oiyama I, OkudaiI N (1986) Production of colchicine-induced autotetraploid plants through micrografting in monoembryonic citrus cultivars. Japan J Breed 36(4):371–376.  https://doi.org/10.1270/jsbbs1951.36.371CrossRefGoogle Scholar
  154. Olivares-Fuster O, Duran-Vila N, Navarro L (2005) Electrochemical protoplast fusion in citrus. Plant Cell Rep 24(2):112–119.  https://doi.org/10.1007/s00299-005-0916-1CrossRefPubMedGoogle Scholar
  155. Oliveira TM, Ben Yahmed J, Dutra J et al (2017) Better tolerance to water deficit in doubled diploid ‘Carrizo citrange’ compared to diploid seedlings is associated with more limited water consumption and better H2O2 scavenging. Acta Physiologiae Plantarum 39:e204Google Scholar
  156. Ollitrault P, Michaux-Ferriere N (1992) Application of flow cytometry for citrus genetic and breeding. Proceeding of the International Citrus Congress, vol 1, pp 193–198Google Scholar
  157. Ollitrault P, Dambier D, Luro F et al (1994) Nuclear genome size variations in Citrus. Fruits (Paris) 49(5/6):390–393, 475–476Google Scholar
  158. Ollitrault P, Allent V, Luro F (1996) Production of haploid plants and embryogenic calli of clementine (Citrus reticulata Blanco) after in situ parthenogenesis induced by irradiated pollen. In: Anonymous proceedings of the international society of Citriculture., vol 2, Sun City, South Africa, pp 913–920Google Scholar
  159. Ollitrault P, Dambier D, Sudahono et al (1996) Somatic hybridization in Citrus: some new hybrid and alloplasmic plants. Proc Int Soc Citric 2:907–912Google Scholar
  160. Ollitrault P, Vanel F, Froelicher Y et al (2000) Creation of triploid citrus hybrids by electrofusion of haploid and diploid protoplasts. Acta Horticulturae 535:191–197Google Scholar
  161. Ollitrault P, Guo W, Grosser J (2007) Recent advances and evolving strategies in citrus somatic hybridization. In: Kahn I (ed) Citrus genetics, breeding and biotechnology. CAB International edn, pp 235–260Google Scholar
  162. Ollitrault P, Froelicher Y, Dambier D et al (2007b) Seedlessness and ploidy manipulations. In: Khan IA (ed) Citrus genetics, breeding and biotechnology. CAB International, Wallingford, pp 197–218CrossRefGoogle Scholar
  163. Ollitrault P, WenWu Guo, Grosser JW (2007c) Somatic hybridization. In: Khan IA (ed) Citrus genetics, breeding and biotechnology. CAB International, Wallingford, pp 235–260CrossRefGoogle Scholar
  164. Ollitrault P, Dambier D, Luro F et al (2008) Ploidy manipulation for breeding seedless triploid citrus. Plant Breed Rev 30:323–352CrossRefGoogle Scholar
  165. Ollitrault P, Terol J, Chen C et al (2012) A reference genetic map of C. clementina hort. ex Tan.; citrus evolution inferences from comparative mapping. BMC Genomics 13:593.  https://doi.org/10.1186/1471-2164-13-593PubMedPubMedCentralCrossRefGoogle Scholar
  166. Ollitrault P, Terol J, Garcia-Lor A et al (2012) SNP mining in C. clementina BAC end sequences; transferability in the Citrus genus (Rutaceae), phylogenetic inferences and perspectives for genetic mapping. BMC Genom 13:13.  https://doi.org/10.1186/1471-2164-13-13PubMedPubMedCentralCrossRefGoogle Scholar
  167. Ollitrault P, Curk F, Ollitrault F et al (2016) Usefulness of phylogentic diagnostic SNP markers of citrus ancestral taxa for genetics and breeding. Book of Abstract; Sustainable Citriculture, The role of applied knowledge International Citrus Congress, pp 126–127Google Scholar
  168. Omar AA, Dutt M, Gmitter FG et al (2016) Somatic embryogenesis: still a relevant technique in citrus improvement. In: Germanà MA, Lambardi M (eds) In vitro embryogenesis in higher plants. Springer, New York, New York, NY, pp 289–327CrossRefGoogle Scholar
  169. Omura M, Shimada T (2016) Citrus breeding, genetics and genomics in Japan. Breed Sci 66(1):3–17.  https://doi.org/10.1270/jsbbs.66.3PubMedPubMedCentralCrossRefGoogle Scholar
  170. Osborn TC, Chris Pires J, Birchler JA et al (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19(3):141–147.  https://doi.org/10.1016/S0168-9525(03)00015-5CrossRefPubMedGoogle Scholar
  171. Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437.  https://doi.org/10.1146/annurev.genet.34.1.401CrossRefPubMedGoogle Scholar
  172. Oueslati A, Salhi-Hannachi A, Luro F et al (2017) Genotyping by sequencing reveals the interspecific C. maxima/C. reticulata admixture along the genomes of modern citrus varieties of mandarins, tangors, tangelos, orangelos and grapefruits. PLoS One 12(10):e0185618.  https://doi.org/10.1371/journal.pone.0185618PubMedPubMedCentralCrossRefGoogle Scholar
  173. Oustric J, Morillon R, Luro F et al (2017) Tetraploid Carrizo citrange rootstock (Citrus sinensis Osb. × Poncirus trifoliata L. Raf.) enhances natural chilling stress tolerance of common clementine (Citrus clementina Hort. ex Tan). J Plant Physiol 214:108–115PubMedCrossRefGoogle Scholar
  174. Oustric J, Morillon R, Ollitrault P et al (2018) Somatic hybridization between diploid Poncirus and Citrus improves natural chilling and light stress tolerances compared with equivalent doubled-diploid genotypes. Trees.  https://doi.org/10.1007/s00468-018-1682-3CrossRefGoogle Scholar
  175. Park T, Kim J, Hutten RCB et al (2007) Genetic positioning of centromeres Using half-tetrad analysis in a 4x × 2x cross population of potato. Genetics 176(1):85–94.  https://doi.org/10.1534/genetics.107.070870CrossRefPubMedPubMedCentralGoogle Scholar
  176. Peloquin SJ, Yerk GL, Werner JE et al (1989) Potato breeding with haploids and 2n gametes. Genome 31(2):1000–1004.  https://doi.org/10.1139/g89-174CrossRefGoogle Scholar
  177. Penjor T, Mimura T, Matsumoto R et al (2014) Characterization of limes (Citrus aurantifolia) grown in Bhutan and Indonesia using high-throughput sequencing. Sci Rep 4:4853PubMedPubMedCentralCrossRefGoogle Scholar
  178. Penjor T, Mimura T, Kotoda N et al (2016) RAD-Seq analysis of typical and minor Citrus accessions, including Bhutanese varieties. Breed Sci 66(5):797–807.  https://doi.org/10.1270/jsbbs.16059
  179. Podda A, Checcucci G, Mouhaya W et al (2013) Salt-stress induced changes in the leaf proteome of diploid and tetraploid mandarins with contrasting Na + and Cl accumulation behaviour. J Plant Physiol 170(12):1101–1112.  https://doi.org/10.1016/j.jplph.2013.03.006PubMedCrossRefPubMedCentralGoogle Scholar
  180. Ramanna MS, Jacobsen E (2003) Relevance of sexual polyploidization for crop improvement A review. Euphytica 133(1):3–8.  https://doi.org/10.1023/A:1025600824483CrossRefGoogle Scholar
  181. Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst 29(1):467–501.  https://doi.org/10.1146/annurev.ecolsys.29.1.467CrossRefGoogle Scholar
  182. Ramsey J, Schemske DW (2002) Neopolyploidy in flowering plants. Annu Rev Ecol Syst 33(1):589–639.  https://doi.org/10.1146/annurev.ecolsys.33.010802.150437CrossRefGoogle Scholar
  183. Reforgiato Recupero G, Russo G, Recupero S (2005) New promising citrus triploid hybrids selected from crosses between monoembryonic diploid female and tetraploid male parents. HortScience 40(3):516–520CrossRefGoogle Scholar
  184. Romero-Aranda R, Bondada BR, Syvertsen JP et al (1997) Leaf characteristics and net gas exchange of diploid and autotetraploid citrus. Ann Bot 79(2):153–160CrossRefGoogle Scholar
  185. Rouiss H, Cuenca J, Navarro L et al (2017a) Tetraploid citrus progenies arising from FDR and SDR unreduced pollen in 4x × 2x hybridizations. Tree Genet Genom 13(1):10.  https://doi.org/10.1007/s11295-016-1094-8CrossRefGoogle Scholar
  186. Rouiss H, Cuenca J, Navarro L et al (2017) Unreduced megagametophyte production in lemon occurs via three meiotic mechanisms, predominantly second-division restitution. Front Plant Sci 8:1211.  https://doi.org/10.3389/fpls.2017.01211
  187. Rouiss H, Bakry F, Froelicher Y et al (2018) Origin of C. latifolia and C. aurantiifolia triploid limes; the preferential disomic inheritance of doubled-diploid ‘Mexican’ lime is consistent with an interploid hybridization hypothesis. Ann Bot 121(3):571–585PubMedCentralCrossRefGoogle Scholar
  188. Ruiz M, Quinones A, Marti-nez-Alcantara B et al (2016a) Effects of salinity on diploid (2x) and doubled diploid (4x) Citrus macrophylla genotypes. Sci Hortic 207:33–40.  https://doi.org/10.1016/j.scienta.2016.05.007CrossRefGoogle Scholar
  189. Ruiz M, Quinones A, Marti-nez-Cuenca MR et al (2016b) Tetraploidy enhances the ability to exclude chloride from leaves in carrizo citrange seedlings. J Plant Physiol 205:1–10.  https://doi.org/10.1016/j.jplph.2016.08.002CrossRefPubMedPubMedCentralGoogle Scholar
  190. Ruiz M, Quinones A, Marti-nez-Alcantara B et al (2016) Tetraploidy enhances boron-excess tolerance in carrizo citrange (Citrus sinensis L. Osb. Poncirus trifoliata L. Raf.). Front Plant Sci 7:701.  https://doi.org/10.3389/fpls.2016.00701
  191. Ruiz M, Pensabene-Bellavia G, Quinones A et al (2018) Molecular characterization and stress tolerance evaluation of new allotetraploid somatic hybrids between Carrizo citrange and Citrus macrophylla W. rootstocks. Front Plant Sci.  https://doi.org/10.3389/fpls.2018.00901
  192. Russo F, Torrisi M (1951) Il polliploidismo nei Citrus Autopoliploidi ed allopoliploidi. Ann Sper Agr 5:1041–1062Google Scholar
  193. Saleh B, Allario T, Dambier D et al (2008) Tetraploid citrus rootstocks are more tolerant to salt stress than diploid. C R Biol 331(9):703–710.  https://doi.org/10.1016/j.crvi.2008.06.007CrossRefPubMedPubMedCentralGoogle Scholar
  194. Sanford J (1983) Ploidy manipulations. In: Moore J, Janick J (eds) Methods in fruit breeding. Purdue University Press, West Lafayette, pp 100–123Google Scholar
  195. Shen X, Gmitter FG, Grosser JW (2011) Immature embryo rescue and culture. In: Thorpe TA, Yeung EC (eds) Plant embryo culture: methods and protocols. Humana Press, Totowa, NJ, pp 75–92CrossRefGoogle Scholar
  196. Shimada T, Fujii H, Endo T et al (2014) Construction of a citrus framework genetic map anchored by 708 gene-based markers. Tree Genet Genom:1–13.  https://doi.org/10.1007/s11295-014-0738-9CrossRefGoogle Scholar
  197. Smykal P (2000) Pollen embryogenesis—the stress mediated switch from gametophytic to sporophytic development. Current status and future prospects. Biol Plant 43(4):481–489.  https://doi.org/10.1023/a:1002835330799CrossRefGoogle Scholar
  198. Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annu Rev Plant Biol 60:561–588.  https://doi.org/10.1146/annurev.arplant.043008.092039CrossRefPubMedPubMedCentralGoogle Scholar
  199. Soltis DE, Soltis PS, Tate JA (2003) Advances in the study of polyploidy since plant speciation. New Phytol 161:173–191CrossRefGoogle Scholar
  200. Soost R (1987) Breeding citrus-genetics and nucellar embryony. In: Abbott A, Atkin R (eds) Improving vegetatively propagated crops. Academic Press, London, pp 83–110Google Scholar
  201. Starrantino A, Reforgiato Recupero G (1981) Citrus hybrids obtained in vitro from 2x females and 4x male. Proc Int Soc Citric 1:31–32Google Scholar
  202. Stebbins GL (1947) Types of polyploids: their classification and significance. Adv Genet 1:403–429.  https://doi.org/10.1016/S0065-2660(08)60490-3CrossRefPubMedPubMedCentralGoogle Scholar
  203. Stebbins G (1971) Chromosomal evolution in higher plants. Addison-Wesley, London, UKGoogle Scholar
  204. Stift M, Berenos C, Kuperus P et al (2008) Segregation models for disomic, tetrasomic and intermediate inheritance in tetraploids: a general procedure applied to Rorippa (Yellow cress) microsatellite data. Genetics 179(4):2113–2123.  https://doi.org/10.1534/genetics.107.085027CrossRefPubMedPubMedCentralGoogle Scholar
  205. Sybenga J (1996) Chromosome pairing affinity and quadrivalent formation in polyploids: do segmental allopolyploids exist? Genome 39(6):1176–1184.  https://doi.org/10.1139/g96-148CrossRefPubMedPubMedCentralGoogle Scholar
  206. Sybenga J (2012) Cytogenetics in plant breeding. Springer, Berlin HeidelbergGoogle Scholar
  207. Syvertsen JP, LEE LS, Grosser JW (2000) Limitations on growth and net gas exchange of diploid and tetraploid Citrus rootstock cultivars grown at elevated CO2. J Am Soc Hort Sci 125(2):228–234CrossRefGoogle Scholar
  208. Szarejko I, Forster BP (2007) Doubled haploidy and induced mutation. Euphytica 158(3):359–370.  https://doi.org/10.1007/s10681-006-9241-1CrossRefGoogle Scholar
  209. Tan F, Tu H, Liang W et al (2015) Comparative metabolic and transcriptional analysis of a doubled diploid and its diploid citrus rootstock (C. junos cv. Ziyang xiangcheng) suggests its potential value for stress resistance improvement. BMC Plant Biology 15:89.  https://doi.org/10.1186/s12870-015-0450-4
  210. Tan F, Tu H, Wang R et al (2017) Metabolic adaptation following genome doubling in citrus doubled diploids revealed by non-targeted metabolomics. Metabolomics 13(11):143.  https://doi.org/10.1007/s11306-017-1276-xCrossRefGoogle Scholar
  211. Tavoletti S, Bingham ET, Yandell BS et al (1996) Half tetrad analysis in alfalfa using multiple restriction fragment length polymorphism markers. Proc Natl Acad Sci 93(20):10918–10922.  https://doi.org/10.1073/pnas.93.20.10918CrossRefPubMedPubMedCentralGoogle Scholar
  212. Terol J, Conesa A, Colmenero JM et al (2007) Analysis of 13000 unique Citrus clusters associated with fruit quality, production and salinity tolerance. BMC Genom 8:31CrossRefGoogle Scholar
  213. Tusa N, Fatta del Bosco S (1997) A new source of Citrus genetic variability: the fertile allotetraploid somatic hybrid breeding parent ‘Valencia sweet orange + Femminello lemon’. Adv Hortic Sci 11(1):55–58Google Scholar
  214. Vardi A, Spiegel-Roy P, Galun E (1982) Plant regeneration from Citrus protoplasts: variability in methodological requirements among cultivars and species. Theor Appl Genet 62(2):171–176.  https://doi.org/10.1007/BF00293354CrossRefPubMedPubMedCentralGoogle Scholar
  215. Vardi A, Levin I, Carmi N (2008) Induction of seedlessness in citrus: from classical techniques to emerging biotechnological approaches. J Am Soc Hortic Sci 133(1):117–126CrossRefGoogle Scholar
  216. Viloria Z, Grosser JW (2005) Acid citrus fruit improvement via interploid hybridization using allotetraploid somatic hybrid and autotetraploid breeding parents. J Am Soc Hortic Sci 130(3):392–402CrossRefGoogle Scholar
  217. Vinson JP, Jaffe DB, O’Neill K et al (2005) Assembly of polymorphic genomes: algorithms and application to Ciona savignyi. Genome Res 15(8):1127–1135.  https://doi.org/10.1101/gr.3722605CrossRefPubMedPubMedCentralGoogle Scholar
  218. Wagner A, Blackstone N, Cartwright P et al (1994) Surveys of gene families using polymerase chain reaction: PCR selection and PCR drift. Syst Biol 43(2):250–261.  https://doi.org/10.2307/2413465CrossRefGoogle Scholar
  219. Wakana A, Hanada N, Min Park S et al (2005) Production of tetraploid forms of acid citrus cultivars by top grafting of shoots with sprouting axially buds treated with colchicine. J Fac Agric Kyushu Univ 50:93–102Google Scholar
  220. Wang M, van Bergen S, Van Duijn B (2000) Insights into a key developmental switch and its importance for efficient plant breeding. Plant Physiol 124(2):523–530PubMedPubMedCentralCrossRefGoogle Scholar
  221. Wang J, Tian L, Madlung A et al (2004) Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. Genetics 167(4):1961–1973.  https://doi.org/10.1534/genetics.104.027896CrossRefPubMedPubMedCentralGoogle Scholar
  222. Wang J, Tian L, Lee HS et al (2006) Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172(1):507–517.  https://doi.org/10.1534/genetics.105.047894CrossRefPubMedPubMedCentralGoogle Scholar
  223. Wang S, Lan H, Cao H et al (2015) Recovery and characterization of homozygous lines from two sweet orange cultivars via anther culture. Plant Cell Tiss Organ Cult (PCTOC) 123(3):633–644.  https://doi.org/10.1007/s11240-015-0866-4CrossRefGoogle Scholar
  224. Wang X, Xu Y, Zhang S et al (2017) Genomic analyses of primitive, wild and cultivated citrus provide insights into asexual reproduction. Nat Genet 49(5):765–772.  https://doi.org/10.1038/ng.3839CrossRefGoogle Scholar
  225. Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42(1):225–249PubMedCrossRefPubMedCentralGoogle Scholar
  226. Winge O (1917) The chromosomes, their numbers and general importance. Compt Rend Trav Lab Carlsberg 13:131–275Google Scholar
  227. Wu J, Mooney P (2002) Autotetraploid tangor plant regeneration from in vitro Citrus somatic embryogenic callus treated with colchicineGoogle Scholar
  228. Wu GA, Prochnik S, Jenkins J et al (2014) Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat Biotechnol 32(7):656–662.  https://doi.org/10.1038/nbt.2906PubMedPubMedCentralCrossRefGoogle Scholar
  229. Wu GA, Terol J, Ibanez V et al (2018) Genomics of the origin and evolution of Citrus. Nature 554:311CrossRefGoogle Scholar
  230. Xiao S, Biswas MK, Li M et al (2014) Production and molecular characterization of diploid and tetraploid somatic cybrid plants between male sterile Satsuma mandarin and seedy sweet orange cultivars. Plant cell and tissue culture 116(1):81–88CrossRefGoogle Scholar
  231. Xie K, Wang X, Biswas MK et al (2014a) 2n megagametophyte formed via SDR contributes to tetraploidization in polyembryonic ‘Nadorcott™ tangor crossed by citrus allotetraploids. Plant Cell Rep 33(10):1641–1650.  https://doi.org/10.1007/s00299-014-1643-2CrossRefPubMedPubMedCentralGoogle Scholar
  232. Xie K, Wang X, Wang H et al (2014b) High efficient and extensive production of triploid citrus plants by crossing polyembryonic diploids with tetraploids. Acta Hortic Sin 41:613–620Google Scholar
  233. Xie K, Xia Q, Wang X et al (2015) Cytogenetic and SSR-marker evidence of mixed disomic, tetrasomic, and intermediate inheritance in a citrus allotetraploid somatic hybrid between ‘Nova’ tangelo and ‘HB’ pummelo. Tree Genet Genom 11(6):112.  https://doi.org/10.1007/s11295-015-0940-4CrossRefGoogle Scholar
  234. Xu Q, Chen L, Ruan X et al (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59–66.  https://doi.org/10.1038/ng.2472CrossRefPubMedPubMedCentralGoogle Scholar
  235. Xu S, Cai D, Tan F et al (2014) Citrus somatic hybrid: an alternative system to study rapid structural and epigenetic reorganization in allotetraploid genomes. Plant Cell, Tissue Organ Cult (PCTOC) 119(3):511–522.  https://doi.org/10.1007/s11240-014-0551-zCrossRefGoogle Scholar
  236. Xu Y, Huang L, Ji D et al (2015) Construction of a dense genetic linkage map and mapping quantitative trait loci for economic traits of a doubled haploid population of Pyropia haitanensis (Bangiales, Rhodophyta). BMC Plant Biol 15(1):228.  https://doi.org/10.1186/s12870-015-0604-4CrossRefPubMedPubMedCentralGoogle Scholar
  237. Yahata M, Nukaya T, Sudo M et al (2015) Morphological characteristics of a doubled haploid line from Banpeiyuâ Pummelo [Citrus maxima (Burm.) Merr.] and its reproductive function. Hortic J 84:30–36.  https://doi.org/10.2503/hortj.MI-005CrossRefGoogle Scholar
  238. Zhang J, Guo W, Zhang T (2002) Molecular linkage map of allotetraploid cotton (Gossypium hirsutum L. Gossypium barbadense L.) with a haploid population. Theor Appl Genet 105(8):1166–1174.  https://doi.org/10.1007/s00122-002-1100-4PubMedCrossRefPubMedCentralGoogle Scholar
  239. Zhang H, Tan E, Suzuki Y et al (2014) Dramatic improvement in genome assembly achieved using doubled-haploid genomes. Sci Rep 4:6780PubMedPubMedCentralCrossRefGoogle Scholar
  240. Zhang X, Mizukoshi M, Zhang H et al (2018) Ultrahigh-density linkage map construction using low-coverage whole-genome sequencing of a doubled haploid population: case study of Torafugu (Takifugu rubripes). Genes 9(3).  https://doi.org/10.3390/genes9030120PubMedCentralCrossRefGoogle Scholar
  241. Zhao H, Speed TP (1998) Statistical analysis of half-tetrads. Genetics 150(1):473PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Patrick Ollitrault
    • 1
    Email author
  • Maria Antonietta Germanà
    • 2
  • Yann Froelicher
    • 1
  • Jose Cuenca
    • 3
  • Pablo Aleza
    • 3
  • Raphaël Morillon
    • 4
  • Jude W. Grosser
    • 5
  • Wenwu Guo
    • 6
  1. 1.CIRAD, UMR AGAP (Univ Montpellier, CIRAD, INRA Montpellier SupAgro)San NicolaoFrance
  2. 2.Dipartimento di Scienze Agrarie, Alimentari e ForestaliUniversità degli Studi di PalermoPalermoItaly
  3. 3.Centro de Citricultura y Producción Vegetal, Instituto Valenciano de Investigaciones Agrarias (IVIA)ValenciaSpain
  4. 4.CIRAD, UMR AGAP (Univ Montpellier, CIRAD, INRA Montpellier SupAgro)Petit BourgFrance
  5. 5.Horticultural Sciences Department, Citrus Research and Education CenterUniversity of Florida/IFASLake AlfredUSA
  6. 6.Key Laboratory of Horticultural Plant Biology (Ministry of Education)Huazhong Agricultural UniversityWuhanChina

Personalised recommendations