Journal of Plant Biotechnology

The Korean Society of Plant Biotechnology (한국식물생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Rediscovery of haploid breeding in the genomics era

유전체 시대에 반수체 육종의 재발견

  • Lee, Seulki (Genomics Division, Department of Agricultural Biotechnology, National Academy of Agricultural Science, Rural Development Administration) ;
  • Kim, Jung Sun (Genomics Division, Department of Agricultural Biotechnology, National Academy of Agricultural Science, Rural Development Administration) ;
  • Kang, Sang-Ho (Genomics Division, Department of Agricultural Biotechnology, National Academy of Agricultural Science, Rural Development Administration) ;
  • Sohn, Seong-Han (Genomics Division, Department of Agricultural Biotechnology, National Academy of Agricultural Science, Rural Development Administration) ;
  • Won, So Youn (Genomics Division, Department of Agricultural Biotechnology, National Academy of Agricultural Science, Rural Development Administration)
  • 이슬기 (농촌진흥청 국립농업과학원 농업생명자원부 유전체과) ;
  • 김정선 (농촌진흥청 국립농업과학원 농업생명자원부 유전체과) ;
  • 강상호 (농촌진흥청 국립농업과학원 농업생명자원부 유전체과) ;
  • 손성한 (농촌진흥청 국립농업과학원 농업생명자원부 유전체과) ;
  • 원소윤 (농촌진흥청 국립농업과학원 농업생명자원부 유전체과)
  • Received : 2015.11.26
  • Accepted : 2016.01.12
  • Published : 2016.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Advances in DNA sequencing technologies have contributed to revolutionary understanding of many fundamental biological processes. With unprecedented cost-effective and high-throughput sequencing, a single laboratory can afford to de novo sequence the whole genome for species of interest. In addition, population genetic studies have been remarkably accelerated by numerous molecular markers identified from unbiased genome-wide sequences of population samples. As sequencing technologies have evolved very rapidly, acquiring appropriate individual plants or populations is a major bottleneck in plant research considering the complex nature of plant genome, such as heterozygosity, repetitiveness, and polyploidy. This challenge could be overcome by the old but effective method known as haploid induction. Haploid plants containing half of their sporophytic chromosomes can be rapidly generated mainly by culturing gametophytic cells such as ovules or pollens. Subsequent chromosome doubling in haploid plants can generate stable doubled haploid (DH) with perfect homozygosity. Here, classical methodology to generate and identify haploid plants or DH are summarized. In addition, haploid induction by epigenetic regulation of centromeric histone is explained. Furthermore, the utilization of haploid plant in the genomics era is discussed in the aspect of genome sequencing project and population genetic studies.

DNA 염기서열 분석기술의 진보는 많은 근본적인 생명현상을 이해하는데 기여해왔다. 유례없는 저비용에 염기서열을 대량으로 분석을 할 수 있게 되어 단일 규모의 실험실에서도 관심이 있는 종의 신규유전체를 해독할 수 있다. 게다가 유전집단의 전체 염기서열을 편향되지 않은 채 분석하여 무수한 분자마커를 발굴할 수 있게 됨에 따라 집단유전학 연구도 두드러지게 가속화되어 왔다. 그러나 식물의 유전체가 이형접합성, 반복염기서열, 배수성과 같은 복잡한 특성이 있다는 것을 고려해 볼 때 기술이 매우 빠르게 진화함에 따라 적절한 개체 혹은 집단을 확보하는 것이 식물 연구에서 주요한 문제가 되었다. 이러한 난제는 오래되었지만 매우 효율적인 기술인 반수체 육성을 통하여 극복될 수 있을 것이다. 정상적인 개체가 갖는 염색체의 절반을 보유하는 반수체 식물은 주로 자방이나 화분과 같은 배우체 세포를 배양함으로써 빠르게 구축될 수 있다. 뒤이은 반수체 식물의 염색체 배수화는 완벽한 동형접합성을 보이는 안정된 배가반수체를 만든다. 본 논문에서는 반수체 식물을 육성하고 판별하기 위한 고전적인 방법론을 요약할 것이다. 게다가 동원체의 히스톤을 후성적으로 조절함으로써 반수체를 유도하는 방법을 설명할 것이다. 마지막으로, 유전체 시대에 반수체 식물의 활용 방안을 유전체 해독과 집단 유전학의 측면에서 논의할 것이다.

Keywords

References

  1. Bandillo N, Raghavan C, Muyco PA, Sevilla MAL, Lobina IT, Dilla-Ermita CJ, Tung C-W, McCouch S, Thomson M, Mauleon R (2013) Multi-parent advanced generation inter-cross (MAGIC) populations in rice: progress and potential for genetics research and breeding. Rice 6:11 https://doi.org/10.1186/1939-8433-6-11
  2. Blakeslee AF, Belling J, Farnham ME, Bergner AD (1922) A haploid mutant in the jimson weed, "Datura Stramonium". Science 55:646-647 https://doi.org/10.1126/science.55.1433.646
  3. Consortium PGS (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189-195 https://doi.org/10.1038/nature10158
  4. D'Hont A, Denoeud F, Aury J-M, Baurens F-C, Carreel F, Garsmeur O, Noel B, Bocs S, Droc G, Rouard M (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213-217 https://doi.org/10.1038/nature11241
  5. Denoeud F, Carretero-Paulet L, Dereeper A, Droc G, Guyot R, Pietrella M, Zheng C, Alberti A, Anthony F, Aprea G (2014) The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science 345:1181-1184 https://doi.org/10.1126/science.1255274
  6. Diao W-P, Jia Y-Y, Song H, Zhang X-Q, Lou Q-F, Chen J-F (2009) Efficient embryo induction in cucumber ovary culture and homozygous identification of the regenerants using SSR markers. Scientia horticulturae 119:246-251 https://doi.org/10.1016/j.scienta.2008.08.016
  7. Dohm JC, Minoche AE, Holtgrawe D, Capella-Gutierrez S, Zakrzewski F, Tafer H, Rupp O, Sorensen TR, Stracke R, Reinhardt R, Goesmann A, Kraft T, Schulz B, Stadler PF, Schmidt T, Gabaldon T, Lehrach H, Weisshaar B, Himmelbauer H (2014) The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature 505:546-549 https://doi.org/10.1038/nature12817
  8. Ferrie AMR, Epp DJ, Keller WA (1995) Evaluation of Brassica rapa L. genotypes for microspore culture response and identification of a highly embryogenic line. Plant Cell Reports 14:580-584
  9. Garcia-Mas J, Benjak A, Sanseverino W, Bourgeois M, Mir G, Gonzalez VM, Henaff E, Camara F, Cozzuto L, Lowy E (2012) The genome of melon (Cucumis melo L.). Proceedings of the National Academy of Sciences 109:11872-11877 https://doi.org/10.1073/pnas.1205415109
  10. Guha S, Maheshwari SC (1964) In vitro production of embryos from anthers of datura. Nature 204:497-497
  11. Guha S, Maheshwari SC (1966) Cell division and differentiation of embryos in the pollen grains of datura in vitro. Nature 212:97-98 https://doi.org/10.1038/212097a0
  12. Han D-S, Niimi Y, Nakano M (1997) Regeneration of haploid plants from anther cultures of the Asiatic hybrid lily 'Connecticut King'. Plant cell, tissue and organ culture 47:153-158 https://doi.org/10.1007/BF02318951
  13. Hofinger BJ, Huynh OA, Jankowicz-Cieslak J, Müller A, Otto I, Kumlehn J, Till BJ (2013) Validation of doubled haploid plants by enzymatic mismatch cleavage. Plant methods 9:43 https://doi.org/10.1186/1746-4811-9-43
  14. Huang BE, George AW, Forrest KL, Kilian A, Hayden MJ, Morell MK, Cavanagh CR (2012) A multiparent advanced generation inter-cross population for genetic analysis in wheat. Plant biotechnology journal 10:826-839 https://doi.org/10.1111/j.1467-7652.2012.00702.x
  15. Huang BE, Verbyla K, Verbyla A, Raghavan C, Singh V, Gaur P, Leung H, Varshney R, Cavanagh C (2015) MAGIC populations in crops: current status and future prospects. Theor Appl Genet 128:999-1017 https://doi.org/10.1007/s00122-015-2506-0
  16. Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P (2009) The genome of the cucumber, Cucumis sativus L. Nature genetics 41:1275-1281 https://doi.org/10.1038/ng.475
  17. Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463-467 https://doi.org/10.1038/nature06148
  18. Kasha K, Kao K (1970) High frequency haploid production in barley (Hordeum vulgare L.). Nature 225:874-876 https://doi.org/10.1038/225874a0
  19. Kim K-M, Nam W-I, Kwon Y-S, Sohn J-K (2004) Development of doubled-haploid population and construction of genetic map using SSR markers in rice. Korean J Plant Biotechnol 31:179-184 https://doi.org/10.5010/JPB.2004.31.3.179
  20. Kover PX, Valdar W, Trakalo J, Scarcelli N, Ehrenreich IM, Purugganan MD, Durrant C, Mott R (2009) A multiparent advanced generation inter-cross to fine-map quantitative traits in Arabidopsis thaliana. PLoS Genet 5:e1000551 https://doi.org/10.1371/journal.pgen.1000551
  21. Kristiansen K, Andersen S (1993) Effects of donor plant temperature, photoperiod, and age on anther culture response of Capsicum annuum L. Euphytica 67:105-109 https://doi.org/10.1007/BF00022732
  22. Lu CS, Sharma HC, Ohm HW (1991) Wheat anther culture: effect of genotype and environmental conditions. Plant Cell, Tissue and Organ Culture 24:233-236 https://doi.org/10.1007/BF00033482
  23. Mackay IJ, Bansept-Basler P, Barber T, Bentley AR, Cockram J, Gosman N, Greenland AJ, Horsnell R, Howells R, O'Sullivan DM (2014) An eight-parent multiparent advanced generation inter-cross population for winter-sown wheat: creation, properties, and validation. G3: $Genes{\mid}\;Genomes{\mid}\;Genetics$ 4:1603-1610
  24. Maheshwari S, Tan EH, West A, Franklin F, Comai L, Chan S (2015) Naturally occurring differences in CENH3 affect chromosome segregation in zygotic mitosis of hybrids. PLoS genetics 11:e1004970-e1004970 https://doi.org/10.1371/journal.pgen.1004970
  25. Malik MR, Wang F, Dirpaul JM, Zhou N, Hammerlindl J, Keller W, Abrams SR, Ferrie AMR, Krochko JE (2008) Isolation of an embryogenic line from non-embryogenic Brassica napus cv. Westar through microspore embryogenesis. Journal of Experimental Botany 59:2857-2873 https://doi.org/10.1093/jxb/ern149
  26. McKone MJ, Halpern SL (2003) The Evolution of Androgenesis. The American Naturalist 161:641-656 https://doi.org/10.1086/368291
  27. Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Saw JH, Senin P, Wang W, Ly BV, Lewis KL (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991-996 https://doi.org/10.1038/nature06856
  28. Mohammadi PP, Moieni A, Ebrahimi A, Javidfar F (2012) Doubled haploid plants following colchicine treatment of microsporederived embryos of oilseed rape (Brassica napus L.). Plant Cell, Tissue and Organ Culture 108:251-256 https://doi.org/10.1007/s11240-011-0036-2
  29. Murovec J, Bohanec B (2011) Haploids and doubled haploids in plant breeding, p. 87-106. In: I.Y. Abdurakhmonov (ed.). Plant Breeding. InTech, Croatia.
  30. Murovec J, Bohanec B (2013) Haploid induction in Mimulus aurantiacus Curtis obtained by pollination with gamma irradiated pollen. Scientia Horticulturae 162:218-225 https://doi.org/10.1016/j.scienta.2013.08.012
  31. Niizeki H, Oono K (1968) Induction of haploid rice plant from anther culture. Proceedings of the Japan Academy 44:554-557
  32. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin Y-C, Scofield DG, Vezzi F, Delhomme N, Giacomello S, Alexeyenko A (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497:579-584 https://doi.org/10.1038/nature12211
  33. Park C-H, Lee M-S, Choi D-G, Cho J-H, Hyun S-W, Hwang C-J, So J-D, Choi B-J (1990) Effect of pollen stage and growth regulators on anther culture of Pulsatilla koreana Nakai. Korean J Plant Tissue Culture 17:239-248
  34. Pascual L, Desplat N, Huang BE, Desgroux A, Bruguier L, Bouchet JP, Le QH, Chauchard B, Verschave P, Causse M (2015) Potential of a tomato MAGIC population to decipher the genetic control of quantitative traits and detect causal variants in the resequencing era. Plant biotechnology journal 13:565-577 https://doi.org/10.1111/pbi.12282
  35. Pathirana R, Frew T, Hedderley D, Timmerman-Vaughan G, Morgan E (2011) Haploid and doubled haploid plants from developing male and female gametes of Gentiana triflora. Plant cell reports 30:1055-1065 https://doi.org/10.1007/s00299-011-1012-3
  36. Qin X, Rotino GL (1995) Chloroplast number in guard cells as ploidy indicator of in vitro-grown androgenic pepper plantlets. Plant Cell, Tissue and Organ Culture 41:145-149 https://doi.org/10.1007/BF00051583
  37. Ravi M, Chan SW (2010) Haploid plants produced by centromeremediated genome elimination. Nature 464:615-618 https://doi.org/10.1038/nature08842
  38. Ryu J-H, Doo H-S, Kwon T-H (1992) Induction of haploid plants by anther culture in sesame. Korean J Plant Tissue Culture 19:171-177
  39. San Noeum L (1976) Haploides d'Hordeum vulgare L. par culture in vitro d'ovaries non fecondes. Ann Amelior Plant 26:751-754
  40. Sannemann W, Huang BE, Mathew B, Leon J (2015) Multi-parent advanced generation inter-cross in barley: high-resolution quantitative trait locus mapping for flowering time as a proof of concept. Molecular Breeding 35:1-16 https://doi.org/10.1007/s11032-015-0202-z
  41. Seguí-Simarro J (2010) Androgenesis Revisited. Bot Rev 76:377-404 https://doi.org/10.1007/s12229-010-9056-6
  42. Seymour DK, Filiault DL, Henry IM, Monson-Miller J, Ravi M, Pang A, Comai L, Chan SW, Maloof JN (2012) Rapid creation of Arabidopsis doubled haploid lines for quantitative trait locus mapping. Proceedings of the National Academy of Sciences 109:4227-4232 https://doi.org/10.1073/pnas.1117277109
  43. Shrestha S, Kang W-H (2009) Effect of genotype of donor plants on the success of anther culture in sweet pepper (Capsicum annuum L.). Korean Journal of Plant Resources 22:506-512
  44. Smith R, Kamp M, Davies R (1981) Reduced plant size of haploid african violets. In Vitro 17:385-387 https://doi.org/10.1007/BF02626736
  45. Tang F, Tao Y, Zhao T, Wang G (2006) In vitro production of haploid and doubled haploid plants from pollinated ovaries of maize (Zea mays). Plant cell, tissue and organ culture 84:233-237 https://doi.org/10.1007/s11240-005-9017-7
  46. Thomas TD (2008) The role of activated charcoal in plant tissue culture. Biotechnology Advances 26:618-631 https://doi.org/10.1016/j.biotechadv.2008.08.003
  47. Upadhyay A, Chacko A, Gandhimathi A, Ghosh P, Harini K, Joseph A, Joshi A, Karpe S, Kaushik S, Kuravadi N, Lingu C, Mahita J, Malarini R, Malhotra S, Malini M, Mathew O, Mutt E, Naika M, Nitish S, Pasha S, Raghavender U, Rajamani A, Shilpa S, Shingate P, Singh H, Sukhwal A, Sunitha M, Sumathi M, Ramaswamy S, Gowda M, Sowdhamini R (2015) Genome sequencing of herb Tulsi (Ocimum tenuiflorum) unravels key genes behind its strong medicinal properties. BMC Plant Biology 15:212 https://doi.org/10.1186/s12870-015-0562-x
  48. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D (2010) The genome of the domesticated apple (Malus $\times$ domestica Borkh.). Nature genetics 42:833-839 https://doi.org/10.1038/ng.654
  49. Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F, Zhebentyayeva T, Dettori MT, Grimwood J, Cattonaro F (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nature genetics 45:487-494 https://doi.org/10.1038/ng.2586
  50. Wang H, Dong B, Jiang J, Fang W, Guan Z, Liao Y, Chen S, Chen F (2014) Characterization of in vitro haploid and doubled haploid Chrysanthemum morifolium plants via unfertilized ovule culture for phenotypical traits and DNA methylation pattern. Frontiers in plant science 5:738
  51. Wedzony M, Forster BP, Zur I, Golemiec E, Szechynska-Hebda M, Dubas E, Gotebiowska G, Wedzony M (2009) Progress in doubled haploid technology in higher plants, p 1-33. In: A. Touraev, B. Forster, SM Jain (eds). Advances In Haploid Production In Higher Plants. Springer, Netherlands.
  52. Xiao L, Yang G, Zhang L, Yang X, Zhao S, Ji Z, Zhou Q, Hu M, Wang Y, Chen M (2015) The resurrection genome of Boea hygrometrica: A blueprint for survival of dehydration. Proceedings of the National Academy of Sciences 112:5833-5837 https://doi.org/10.1073/pnas.1505811112
  53. Zeng X, Long H, Wang Z, Zhao S, Tang Y, Huang Z, Wang Y, Xu Q, Mao L, Deng G (2015) The draft genome of Tibetan hulless barley reveals adaptive patterns to the high stressful Tibetan Plateau. Proceedings of the National Academy of Sciences 112:1095-1100 https://doi.org/10.1073/pnas.1423628112
  54. Zhang H, Tan E, Suzuki Y, Hirose Y, Kinoshita S, Okano H, Kudoh J, Shimizu A, Saito K, Watabe S, Asakawa S (2014) Dramatic improvement in genome assembly achieved using doubled-haploid genomes. Scientific Reports 4:6780 https://doi.org/10.1038/srep06780
  55. Zhang X, Wu Q, Li X, Zheng S, Wang S, Guo L, Zhang L, Custers JB (2011) Haploid plant production in Zantedeschia aethiopica 'Hong Gan' using anther culture. Scientia horticulturae 129:335-342 https://doi.org/10.1016/j.scienta.2011.03.045