Advertisement

Tree Genetics & Genomes

, 15:23 | Cite as

Low temperature increases the frequency of 2n female gametes in the diploid rubber tree (Hevea brasiliensis (Willd. ex A.Juss.) Müll. Arg.)

  • Zhang Yuan-yuan Email author
  • Zhang Xiao-fei 
  • Huang Xiao 
  • Zhang Xiao-yun 
  • Yao Peng-qiang 
  • Li Wei-guo 
Original Article
  • 86 Downloads
Part of the following topical collections:
  1. Adaptation

Abstract

Triploid breeding via the fusion of 2n gametes and n gametes is an efficient method for breeding new varieties in woody plants. Triploid plants are frequently observed in the seedlings of the diploid rubber clone GT1. However, the factors affecting the occurrence and source of triploid progeny in GT1 are still unknown. In this study, the correlation between temperature and triploid progeny frequency in GT1 in different environments over 6 years was analyzed to evaluate the influence of temperature on the frequency of 2n female gametes. A total of 76 triploid progenies were analyzed using 19 simple sequence repeat markers, with the aim of revealing their genetic origin and the mechanism underlying 2n megagametophyte formation. The results showed that low temperature increased the frequency of triploid progeny in GT1, and the determination of allelic status revealed that all triploids were derived from the 2n female gametes, thereby confirming that low temperature increased the frequency of 2n female gametes. The rate of maternal heterozygosity restitution (HR) of seven loci varied from 2.70 to 67.65% with a mean value of 40.56%, and the rate of maternal HR of 37 triploids varied from 14.29 to 66.67% with a mean value of 41.38%, indicating that the production of 2n eggs in the triploid seedlings of GT1 was by second division restitution. The results of this study are valuable for the polyploid breeding of rubber trees.

Keywords

Hevea brasiliensis Triploids Low temperature SSR 2n gametes SDR 

Notes

Acknowledgments

We would like to acknowledge the members of our laboratories for advice. We thank the Yunnan Institute of Tropical Crops, Dehong Institute of Tropical Agricultural Sciences of Yunnan Province and Comprehensive Service Center of Mengla Farm, State Farms Bureau of Yunnan, for collecting the plant material and for additional help. We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.

Data archiving statement

SSR markers used in this study are from the published papers (Souza et al. 2009; An et al. 2009, 2013; Triwitayakorn et al. 2011; Li et al. 2012). Information about of all the applied SSR markers is available in Table 2. The data of triploid frequency for Jinghong2010 and Jinghong2012 were referenced from the literature (Zhang 2013), which are available in CNKI (http://cnki.net/).

Author contributions

Conceived and designed the experiments: Yuan-yuan Zhang, Wei-guo Li; performed the experiments: Yuan-yuan Zhang, Xiao-fei Zhang, Xiao Huang; contributed materials/analysis tools: Yuan-yuan Zhang, Peng-Qiang Yao; wrote the paper: Yuan-yuan Zhang.

Funding information

This research was funded by Hainan Provincial Department of Science and Technology (317281) and Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (No. 1630022017010).

Supplementary material

11295_2019_1330_MOESM1_ESM.docx (25 kb)
ESM 1 (DOCX 25 kb)
11295_2019_1330_MOESM2_ESM.docx (49 kb)
ESM 2 (DOCX 48 kb)

References

  1. Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141.  https://doi.org/10.1016/j.pbi.2005.01.001 CrossRefPubMedGoogle Scholar
  2. An ZW, Zhao YH, Cheng H, Li WG, Huang HS (2009) Development and application of EST-SSR markers in Hevea brasiliensis Muell. Arg. Hereditas 31(3):311–319 (in Chinese with English abstract)CrossRefGoogle Scholar
  3. An ZW, Li YC, Zhai QL, Xie LL, Zhao YH, Huang HS (2013) Development and characterization of novel expressed sequence tag-derived simple sequence repeat markers in Hevea brasiliensis (rubber tree). Genet Mol Res 12(4):5905–5910.  https://doi.org/10.1007/s11032-016-0461-3 CrossRefPubMedGoogle Scholar
  4. Ao SC, He LG, Xiao GX, Chen JB, He CG (1998) Selection of rubber cold fast and high-yield strains, Yunyan77–2 and Yunyan 77–2. Journal of Yunnan Tropical Crops Science & Technology 21(2): 3–8. (in Chinese with English abstract)Google Scholar
  5. Barone A, Gebhardt C, Frusciante L (1995) Heterozygosity in 2n gametes of potato evaluated by RFLP markers. Theor Appl Genet 91:98–104.  https://doi.org/10.1007/BF00220864 CrossRefPubMedGoogle Scholar
  6. Bretagnolle FA, 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.x CrossRefGoogle Scholar
  7. Chen CX, Lyon TM, O’Malley D, Federici TC, Gmitter J, Grosser WJ, Chaparro XJ, Roose LM, Fmitter GF Jr (2008) Origin and frequency of 2n gametes in Citrus sinensis × Poncirus trifoliata and their reciprocal crosses. Plant Sci 174:1–8.  https://doi.org/10.1016/j.plantsci.2007.08.005. CrossRefGoogle Scholar
  8. Cuenca J, Froelicher Y, Aleza P, Juárez J, Navarro L, Ollitrault P (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 107(5):462–470.  https://doi.org/10.1038/hdy.2011.33 CrossRefPubMedPubMedCentralGoogle Scholar
  9. De Storme N, Geelen D (2013) Sexual polyploidization in plants–cytological mechanisms and molecular regulation. New Phytol 198:670–684.  https://doi.org/10.1111/nph.12184 CrossRefPubMedPubMedCentralGoogle Scholar
  10. De Storme N, Copenhaver GP, Geelen D (2012) Production of diploid male gametes in Arabidopsis by cold-induced destabilization of postmeiotic radial microtubule arrays. Plant Physiol 160:1–19CrossRefGoogle Scholar
  11. Dong CB, Suo YJ, Kang XY (2014) Assessment of the genetic composition of triploid hybrid Populus using SSR markers with low recombination frequencies. Can J For Res 44:692–699.  https://doi.org/10.1139/g83-091 CrossRefGoogle Scholar
  12. Dong CB, Suo YJ, Wang J, Kang XY (2015) Analysis of transmission of heterozygosity by 2n gametes in Populus (Salicaceae). Tree Genet Genomes 11:799.  https://doi.org/10.1007/s11295-014-0799-9 CrossRefGoogle Scholar
  13. Draeger T, Moore G (2017) Short periods of high temperature during meiosis prevent normal meiotic progression and reduce grain number in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 130:1785–1800.  https://doi.org/10.1007/s00122-017-2925-1 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Esselink GD, 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 109:402–408CrossRefGoogle Scholar
  15. Ferrante PS, Lucretti S, Reale S, Patrizio DA, Abbate L, Tusa N, Scarano TM (2010) Assessment of the origin of new citrus tetraploid hybrids (2n=4x) by means of SSR markers and PCR based dosage effects. Euphytica 173:223–233.  https://doi.org/10.1007/s10681-009-0093-3 CrossRefGoogle Scholar
  16. Grosser JW, An HJ, Calovic M, Lee DH, Chen C, Vasconcellos M, Gmitter FG (2010) Production of new allotetraploid and autotetraploid citrus breeding parents, focus on zipperskin mandarins. HortScience 45:1160–1163 http://hortsci.ashspublications.org/content/45/8/1160.full CrossRefGoogle Scholar
  17. Gu XF, Luo ZR (2002) Study on germinant characteristic and radio sensitivity of Giant pollen in Nonastringent Persimmon. J Wuhan Bot Res 20(4):280–282 (in Chinese with English abstract)Google Scholar
  18. Hamzah S, Chan JL, Yeang HY (2002) Pollen tube growth and fruit-set success in Hevea brasiliensis hand-pollination influenced by the choice of clone and female flower. Euphytica 123:1–8CrossRefGoogle Scholar
  19. Hermsen JGT (1984) Mechanisms and genetic implications of 2n gamete formation. Iowa State J Res 58:421–434Google Scholar
  20. Hu DQ, Yuan ML, Wu YT, Liu BY, Lin S, Li YZ, Li DS (1982) Selection and separation of natural polyploid in rubber tree. Chin J Trop Agric 3:1–5 (in Chinese)Google Scholar
  21. Kang XY, Zhu ZT (1997) A study on the 2n pollen vitality and germinant characteristics of white poplars. Acta Bot Yunnanica 19(4):402–406 (in Chinese with English abstract)Google Scholar
  22. Kreiner MJ, Kron P, Husband CB (2017) Frequency and maintenance of unreduced gametes in natural plant populations: associations with reproductive mode, life history and genome size. New Phytol 214:879–889CrossRefGoogle Scholar
  23. Li YH, Kang XY, Wang SD, Zhang ZH, Chen HW (2008) Triploid induction in Populus alba × P. glandulosa by chromosome doubling of female gametes. Silvae Genet 57:37–40.  https://doi.org/10.1515/sg-2008-0006 CrossRefGoogle Scholar
  24. Li HB, Zhou TY, Ning LY, Li GH (2009) Cytological identification and breeding course of Hevea Yunyan77-2 and Yunyan77-4. J Trop Subtrop Bot 17(6):602–605 (in Chinese with English abstract)Google Scholar
  25. Li DJ, Deng D, Qin B, Liu XH, Men ZH (2012) De novo assembly and characterization of bark transcriptome using Illumina sequencing and development of EST-SSR markers in rubber tree (Hevea brasiliensis Muell. Arg.). BMC Genomics 13:192.  https://doi.org/10.1186/1471-2164-13-192 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Li Y, Wang Y, Wang PQ, Yang J, Kang XY (2016) Induction of unreduced megaspores in Eucommia Ulmoides by high temperature treatment during megasporogenesis. Euphytica 212:515–524.  https://doi.org/10.1007/s10681-016-1781-4 CrossRefGoogle Scholar
  27. Li DL, Tian J, Xue YX, Chen HW, Wang J (2019) Triploid production via heat-induced diploidization of megaspores in Populus pseudo-simonii. Euphytica 215(10).  https://doi.org/10.1007/s10681-018-2330-0
  28. Liesebach H, Ulrich K, Ewald D (2015) FDR and SDR processes in meiosis and diploid gamete formation in poplars (Populus L.) detected by centromere-associated microsatellite markers. Tree Genet Genomes 11(801).  https://doi.org/10.1007/s11295-014-0801-6
  29. Luca C (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6(11):836–846.  https://doi.org/10.1038/nrg1711 CrossRefGoogle Scholar
  30. Mason AS, Pires JC (2015) Unreduced gametes: meiotic mishap or evolutionary mechanism? Trends Genet 31(1):5–10.  https://doi.org/10.1016/j.tig.2014.09.011 CrossRefPubMedGoogle Scholar
  31. Mason SS, Nelson NM, Yan GJ, Cowling AW (2011) Production of viable male unreduced gametes in Brassica interspecific hybrids is genotype specific and stimulated by cold temperatures. BMC Plant Biol 11:103.  https://doi.org/10.1186/1471-2229-11-103 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Mchale NA (1983) Environmental induction of high frequency 2n pollen formation in diploid Solanum. Can J Genet Cytol 25(6):609–615CrossRefGoogle Scholar
  33. Mendiburu A, Peloquin S (1977a) The significance of 2n gametes in potato breeding. Theor Appl Genet 49:53–61CrossRefGoogle Scholar
  34. Mendiburu AO, Peloquin S (1977b) Bilateral sexual polyploidization in potatoes. Euphytica 26:573–583CrossRefGoogle Scholar
  35. Mooibroek H, Cornish K (2000) Alternative sources of natural rubber. Appl Microbiol Biotechnol 53:355–365.  https://doi.org/10.1007/s002530051627 CrossRefPubMedGoogle Scholar
  36. Navarro L, Aleza P, Cuenca J, Juárez J, Pina JA, Ortega C et al (2015) The mandarin triploid breeding program in Spain. Acta Hortic 1065:389–396.  https://doi.org/10.17660/ActaHortic.2015.1065.48 CrossRefGoogle Scholar
  37. Omokhafe KO, Nasiru I (2005) Genetic improvement of Hevea brasiliensis in Nigeria. In: Mathew NM, Jacob CK, Nair MGS, Thomas KK, Satisha GC, Srinivas P, Korah AC et al (eds) Proceedings of the international natural rubber conference, Cochin. Modern Graphics, Indiana, pp 13–17Google Scholar
  38. Osman K, Higgins JD, Sanchez-Moran E, Armstrong SJ, Franklin FC (2011) Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 190:523–544CrossRefGoogle Scholar
  39. Pecrix Y, Rallo G, Folzer H, Cigna M, Gudin S, Le Bris M (2011) Polyploidization mechanisms: temperature environment can induce diploid gamete formation in Rosa sp. J Exp Bot 62:3587–3597CrossRefGoogle Scholar
  40. Peloquin SJ, Boiteux LS, Simon PW, Jansky SH (2008) A chromosome-specific estimate of transmission of heterozygosity by 2n gametes in potato. J Hered 99(2):177–181.  https://doi.org/10.1093/jhered/esm110 CrossRefPubMedGoogle Scholar
  41. Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst 29:467–501CrossRefGoogle Scholar
  42. Rouiss H, Cuenca J, Navarro L, Ollitrault P, Aleza P (2017a) Tetraploid citrus progenies arising from FDR and SDR unreduced pollen in 4x × 2x hybridizations. Tree Genet Genomes 13(1):14.  https://doi.org/10.1007/s11295-016-1094-8 CrossRefGoogle Scholar
  43. Rouiss H, Cuenca J, Navarro L, Ollitrault P, Aleza P (2017b) Unreduced megagametophyte production in lemon occurs via three meiotic mechanisms, predominantly second-division restitution. Front Plant Sci 8:16.  https://doi.org/10.3389/fpls.2017.01211 CrossRefGoogle Scholar
  44. Serapiglia MJ, Gouker FE, Smart LB (2014) Early selection of novel triploid hybrids of shrub willow with improved biomass yield relative to diploids. BMC Plant Biol 14:74.  https://doi.org/10.1186/1471-2229-14-74 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Souza ML, Mantello CC, Santos MO, Goncalves SP, Souza PA (2009) Microsatellites from rubber tree (Hevea brasiliensis) for genetic diversity analysis and cross-amplification in six Hevea wild species. Conserv Genet Resour 1:75–79.  https://doi.org/10.1007/s12686-009-9018-7 CrossRefGoogle Scholar
  46. Triwitayakorn K, Chatkulkawin P, Kanjanawattanawong S, Sraphet S, Yoocha T, Sangsrakru D, Chanprasert J, Ngamphiw C, Jomchai N, Therawattanasuk K, Tangphatsornruang S (2011) Transcriptome sequencing of Hevea brasiliensis for development microsatellite markers and construction of a genetic linkage map. DNA Res 18:471–482.  https://doi.org/10.1093/dnares/dsr034 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Van Beilen BJ, Poirier Y (2007) Establishment of new crops for the production of natural rubber. Trens Biotechnol 25(1):522–529.  https://doi.org/10.1016/j.tibtech.2007.08.009 CrossRefGoogle Scholar
  48. Wang J, Li DL, KANG XY (2012) Induction of unreduced megaspores with high temperature during megasporogenesis in Populus. Ann For Sci 69:59–67CrossRefGoogle Scholar
  49. Wei MM, Li WG, Huang HS, Luo P, He LG (2016) Regional configuration of rubber tree varieties in the main producing areas in China. Chin J Trop Crops 37(8):1634–1643 (in Chinese with English abstract)Google Scholar
  50. Wu CT, Li WG, Gao XS, Zhang XF, Zhang WS (2009) Problems in rubber tree breeding in China and their countermeasures. Acta Agric Jiangxi 21(12):74–77 (in Chinese with English abstract)Google Scholar
  51. Xie KD, Wang XP, Biswas MK, Liang WJ, Xu Q, Grosser JW, Guo WW (2014) 2n megagametophyte formed via SDR contributes to tetraploidization in polyembryonic ‘Nadorcoot’ tangor crossed by citrus allotetraploids. Plant Cell Rep 33(10):1641–1650.  https://doi.org/10.1007/s00299-014-1643-2 CrossRefPubMedGoogle Scholar
  52. Yang J, Wang JZ, Liu Z, Xiong T, Lan J, Han Q, Li Y, Kang XY (2018) Megaspore chromosome doubling in Eucalyptus urophylla S.T. Blake induced by colchicine treatment to produce triploids. Forests 9:728.  https://doi.org/10.3390/f9110728 CrossRefGoogle Scholar
  53. Yao PQ, Li GH, Long QY, He LG, Kang XY (2016) Male parent identification of triploid rubber trees (Hevea brasiliensis) and the mechanism of 2n gametes formation. Forests 7(12):301.  https://doi.org/10.3390/f7120301 CrossRefGoogle Scholar
  54. Zhang Y Y (2013) Disciplines of fruit-set success and triploid induction of Hevea brasiliensis. Dissertation, Beijing Forestry University 2013. (in Chinese with English abstract)Google Scholar
  55. Zhang S, Qi L, Chen C, Li X, Song W, Chen R, Han S (2004) A report of triploid Populus of the section Aigeiros. Silvae Genet 53:69–75CrossRefGoogle Scholar
  56. Zhao SJ (1985) An observation on pollen development of clone GT1. Chin J Trop Crops 6(2):25–27 (in Chinese with English abstract)Google Scholar
  57. Zhu ZT, Lin HB, Kang XY (1995) Studies on allotriploid breeding of Populus Tomentosa B301 clones. Sci Silave Sin 31(6):499–505 (in Chinese with English abstract)Google Scholar
  58. Zhu ZT, Kang XY, Zhang ZT (1997) Advances in the triploid breeding program of Populus Tomentosa in China. J Beijing For Univ 6(2):1–8Google Scholar
  59. Zhu ZT, Kang XY, Zhang ZY (1998) Studies on selection of natural triploid of Populus Tomentosa. Sci Silvae Sin 34:22–31Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Biology and Genetic Resources of Rubber Tree Ministry of AgricultureDanzhouPeople’s Republic of China
  2. 2.State Centre for Rubber BreedingChinese Academy of Tropical Agricultural SciencesDanzhouPeople’s Republic of China
  3. 3.Dehong Institute of Tropical Agricultural Sciences of Yunnan ProvinceRuiliPeople’s Republic of China
  4. 4.Pingdingshan UniversityPingdingshanPeople’s Republic of China

Personalised recommendations