High temperature-induced production of unreduced pollen and its cytological effects in Populus

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Wang, Jun ^a   Li, Daili ^b   Shang, Fengnan ^a   Kang, Xiangyang ^a  

^a BEIJING FORESTRY UNIVERSITY   (China)

^b Beijing Huang Fa Nursery ^*  (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME SEGREGATION; CYTOKINESIS; CYTOLOGY; DIPLOIDY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT; MEIOSIS; METABOLISM; MICROTUBULE; PLANT BREEDING; PLANT CHROMOSOME; POLLEN; POPULUS;

CHROMOSOME SEGREGATION; CHROMOSOMES, PLANT; CYTOKINESIS; DIPLOIDY; HOT TEMPERATURE; MEIOSIS; MICROTUBULES; PLANT BREEDING; POLLEN; POPULUS;

EID: 85023774906     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-05661-x     Document Type: Article

References (63)

1. Van de Peer, Y., Maere, S. & Meyer, A. The evolutionary significance of ancient genome duplications. Nature Rev. Genet. 10, 725-732 (2009).
2. De Storme, N. & Mason, A. Plant speciation through chromosome instability and ploidy change: Cellular mechanisms, molecular factors and evolutionary relevance. Curr. Plant Biol. 1, 10-33 (2014).
3. Jiao, Y. et al. Ancestral polyploidy in seed plants and angiosperms. Nature 473, 97-100 (2011).
4. Barker, M. S., Arrigo, N., Baniaga, A. E., Li, Z. & Levin, D. A. On the relative abundance of autopolyploids and allopolyploids. New Phytol. 210, 391-398 (2016).
5. Chen, Z. J. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu. Rev. Plant Biol. 58, 377-406 (2007).
6. De Storme, N. & Geelen, D. Sexual polyploidization in plants-cytological mechanisms and molecular regulation. New Phytol. 198, 670-684 (2013).
7. Mok, D. W. S. & Peloquin, S. J. Three mechanisms of 2n pollen formation in diploid potatoes. Can. J. Genet. Cytol. 17, 217-225 (1975).
8. Ramanna, M. S. A re-examination of the mechanisms of 2n gamete formation in potato and its implications for breeding. Euphytica 28, 537-561 (1979).
9. Lim, K. B., Ramanna, M. S., de Jong, J. H., Jacobsen, E. & Van Tuyl, J. M. Indeterminate meiotic restitution (IMR): a novel type of meiotic nuclear restitution mechanism detected in interspecific lily hybrids by GISH. Theor. Appl. Genet. 103, 219-230 (2001).
10. Bastiaanssen, H. J. M., V D Berg, P. M. M. M., Lindhout, P., Jacobsen, E. & Ramanna, M. S. Postmeiotic restitution in 2n-egg formation of diploid potato. Heredity 81, 20-27 (1998).
11. Cuenca, J. et al. Maximum-likelihood method identifies meiotic restitution mechanism from heterozygosity transmission of centromeric loci: application in citrus. Sci. Rep. 5, 9897, doi: 10.1038/srep09897 (2015).
12. Brownfield, L. & Köhler, C. Unreduced gamete formation in plants: mechanisms and prospects. J. Exp. Bot. 62, 1659-1668 (2011).
13. Kaul, M. L. H. & Murthy, T. G. K. Mutant genes affecting higher plant meiosis. Theor. Appl. Genet. 70, 449-466 (1985).
14. d'Erfurth, I. et al. Mutations in AtPS1 (Arabidopsis thaliana parallel spindle 1) lead to the production of diploid pollen grains. PLoS Genet. 4, e1000274, doi: 10.1371/journal.pgen.1000274 (2008).
15. De Storme, N. & Geelen, D. The Arabidopsis mutant jason produces unreduced first division restitution male gametes through a parallel/fused spindle mechanism in meiosis II. Plant Physiol. 155, 1403-1415 (2011).
16. Younis, A., Hwang, Y. J. & Lim, K. B. Exploitation of induced 2n-gametes for plant breeding. Plant Cell Rep. 33, 215-223 (2014).
17. Pécrix, Y. et al. Polyploidization mechanisms: temperature environment can induce diploid gamete formation in Rosa sp. J. Exp. Bot. 62, 3587-3597 (2011).
18. Singhal, K. V., Rana, P. K. & Kumar, P. Syncytes during male meiosis resulting in 2n pollen grain formation in Lindelofia longiflora var. falconeri. J. Syst. Evol. 49, 406-410 (2011).
19. Mason, A. S., Nelson, M. N., Yan, G. & Cowling, W. A. Production of viable male unreduced gametes in Brassica interspecific hybrids is genotype specific and stimulated by cold temperatures. BMC Plant Biol. 11, 103, doi: 10.1186/1471-2229-11-103 (2011).
20. Zhang, X. Z. et al. Creating triploid germplasm via induced 2n pollen in Capsicum annuum L. J. Hortic. Sci. Biotech. 78, 84-88 (2002).
21. Nomura, K. et al. Induction of triploidy by heat shock in the Japanese eel Anguilla japonica. Fisheries Sci. 70, 247-255 (2004).
22. Malik, C. P. Effect of variations in temperature on meiosis in Gagea reticulata Schultes. Nature 187, 805-806 (1960).
23. Brown, R. C. & Lemmon, B. E., Pollen development in orchids. 1. Cytoskeleton and the control of division plane in irregular patterns of cytokinesis. Protoplasma 163, 9-18 (1991).
24. Shamina, N. V., Gordeeva, E. I., Kovaleva, N. M., Seriukova, E. G. & Dorogova, N. V. Formation and function of phragmoplast during successive cytokinesis stages in higher plant meiosis. Cell Biol. Int. 31, 626-635 (2007).
25. Wang, J. & Kang, X. Distribution of microtubular cytoskeletons and organelle nucleoids during microsporogenesis in a 2n pollen producer of hybrid. Populus. Silvae Genet. 58, 220-226 (2009).
26. Wang, J., Kang, X. & Zhu, Q. Variation in pollen formation and its cytological mechanism in an allotriploid white poplar. Tree Genet. Genom. 6, 281-290 (2010).
27. De Storme, N. & Geelen, D. Cytokinesis in plant male meiosis. Plant Signal Behav. 8, e23394, doi: 10.4161/psb.23394 (2013).
28. De Storme, N., Copenhaver, G. P. & Geelen, D. Production of diploid male gametes in Arabidopsis by cold-induced destabilization of postmeiotic radial microtubule arrays. Plant Physiol. 160, 1808-1826 (2012).
29. Rae, A. M., Street, N. R. & Rodríguez-Acosta, M. Populus trees. In Forest trees (ed. Kole, C.) 1-28 (Springer, 2007).
30. Nilsson-Ehle, H. Note regarding the gigas form of Populus tremula found in nature. Hereditas 21, 372-382 (1936).
31. Müntzing, A. The chromosomes of a grant Populus tremula. Hereditas 21, 383-393 (1936).
32. Mashkina, O. S., Burdaeva, L. M., Belozerova, M. M. & Vyunova, L. N. Method of obtaining diploid pollen of woody species. Lesovedenie 1, 19-25 (1989).
33. Kang, X. Y., Zhu, Z. T. & Zhang, Z. Y. Suitable period of high temperature treatment for 2n pollen of Populus tomentosa × P. bolleana. J. Beijing For. Univ. 22, 1-4 (2000).
34. Wang, J., Kang, X. Y. & Li, D. L. High temperature-induced triploid production during embryo sac development in. Populus. Silvae Genet. 61, 85-93 (2012).
35. Wang, J., Li, D. L. & Kang, X. Y. Induction of unreduced megaspores with high temperature during megasporogenesis in. Populus. Ann. For. Sci. 69, 59-67 (2012).
36. Li, F. L. & Zhang, Z. Y. High temperature induced large pollen of Populus. Chin. Bull. Bot. 11, 3 (1994).
37. Wang, J., Kang, X., Wei, Q. & Wang, S. Pollen development and floral morphology of Populus pseudo-simonii. For. Stud. China 11, 99-104 (2009).
38. Bretagnolle, F. & Thompson, J. D. Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol. 129, 1-22 (1995).
39. Cramer, C. S. Laboratory techniques for determining ploidy in plants. HortTechnology 9, 594-596 (1999).
40. Wu, J. et al. Comparative cytological and transcriptomic analysis of pollen development in autotetraploid and diploid rice. Plant Reprod. 27, 181-196 (2014).
41. Song, S. et al. Morphological characterization and in vitro germination of heat-treated pollen in Eucommia ulmoides. Silvae Genet. 64, 99-108 (2015).
42. Tondini, F., Tawoletti, S., Mariani, A. & Veronesi, F. A statistical approach to estimate the frequency of n, 2n and 4n pollen grains in diploid alfalfa. Euphytica 69, 109-114 (1993).
43. Zhang, Z. Y., Li, F. L., Zhu, Z. T. & Kang, X. Y. Doubling technology of pollen chromosome of Populus tomentosa and its hybrid. J. Beijing For. Univ. 2, 9-20 (1997).
44. Wahid, A., Gelani, S., Ashraf, M. & Foolad, M. R. Heat tolerance in plants: an overview. Environ. Exp. Bot. 61, 199-223 (2007).
45. Kang, X. Y. Polyploid induction techniques and breeding strategies in poplar. In Polyploidy and hybridization for crop improvement (ed. Mason, A.) 76-96 (CRC Press, 2016).
46. Kang, X. Y., Zhu, Z. T. & Lin, H. B. Study on the effective treating period for pollen chromosome doubling of Populus tomentosa × P. bolleana. Scientia Silvae Sinicae 35, 21-24 (1999).
47. Li, Y. H., Kang, X. Y., Wang, S. D., Zhang, Z. H. & Chen, H. W. Triploid induction in Populus alba × P. glandulosa by chromosome doubling of female gametes. Silvae Genet. 57, 37-40 (2008).
48. Dong, C. B., Suo, Y. J., Wang, J. & Kang, X. Y. Analysis of transmission of heterozygosity by 2n gametes in Populus (Salicaceae). Tree Genet. Genom 11, 799, doi: 10.1007/s11295-014-0799-9 (2015).
49. Hedhly, A., Hormaza, J. I. & Herrero, M. Global warming and sexual plant reproduction. Trends Plant Sci. 14, 30-36 (2009).
50. Bomblies, K., Higgins, J. D. & Yant, L. Meiosis evolves: adaptation to external and internal environments. New Phytol. 208, 306-323 (2015).
51. Sage, T. L. et al. The effect of high temperature stress on male and female reproduction in plants. Field Crops Res. 182, 30-42 (2015).
52. Hesse, M. & Hess, M. W. Recent trends in tapetum research. A cytological and methodological review. In The tapetum (eds. Hesse, M., Pacini, E. & Willemse, M.) 127-145 (Springer, 1993).
53. Suzuki, K., Takeda, H., Tsukaguchi, T. & Egawa, Y. Ultrastructural study on degeneration of tapetum in anther of snap bean (Phaseolus vulgaris L.) under heat stress. Sex. Plant Reprod. 13, 293-299 (2001).
54. 1 pollen sterility loci and abnormal chromosome behaviour caused pollen sterility in intersubspecific autotetraploid rice hybrids. J. Exp. Bot. 62, 4433-4445 (2011).
55. Zhang, Z. H. & Kang, X. Y. Cytological characteristics of numerically unreduced pollen production in Populus tomentosa Carr. Euphytica 173, 151-159 (2010).
56. Henry, I. M., Zinkgraf, M. S., Groover, A. T. & Comai, L. A system for dosage-based functional genomics in poplar. Plant Cell 27, 2370-2383 (2015).
57. Brown, R. C. & Lemmon, B. E. Minispindles and cytoplasmic domains in microsporogenesis of Orchids. Protoplasma 148, 26-32 (1989).
58. Li, Y., Guo, Q., Wang, J., Tian, J. & Kang, X. Y. Colchicine-induced pollen chromosome doubling and its cytological effects in Populus alba L. J. Nucl. Agri. Sci. 28, 749-756 (2014).
59. Brinkley, B. R. Microtubule organizing centers. Annu. Rev. Cell Biol. 1, 145-172 (1985).
60. Zhu, Z. T., Lin, H. B. & Kang, X. Y. Studies on allotriploid breeding of Populus tomentosa B301 clones. Sci. Silvae Sinicae 31, 499-505 (1995).
61. Zhang, S. et al. A report of triploid Populus of the section Aigeiros. Silvae Genet. 53, 69-75 (2004).
62. Zhang, S. G. et al. Chromosome numbers of some Populus taxa from China. Acta Phytotaxonomica Sinica 43, 539-544 (2005).
63. R Development Core Team. R: a language and environment for statistical computing. (Austria R Foundation for Statistical Computing 2007).