The cohesin loader SCC2 contains a PHD finger that is required for meiosis in land plants

Autoři: Hongkuan Wang aff001;  Wanyue Xu aff001;  Yujin Sun aff003;  Qichao Lian aff001;  Cong Wang aff001;  Chaoyi Yu aff001;  Chengpeng He aff001;  Jun Wang aff001;  Hong Ma aff004;  Gregory P. Copenhaver aff003;  Yingxiang Wang aff001
Působiště autorů: State Key Laboratory of Genetic Engineering and Ministry of Education Key Laboratory of Biodiversity Sciences and Ecological Engineering, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, China aff001;  Center for Epigenetics, Van Andel Institute, Grand Rapids, Michigan, United States of America aff002;  Department of Biology and the Integrative Program for Biological and Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America aff003;  Department of Biology, the Huck Institutes of the Life Sciences, the Pennsylvania State University, University Park, Pennsylvania, United States of America aff004;  Lineberger Comprehensive Cancer Center, University of North Carolina School of Medicine, Chapel Hill, North Carolina, United States of America aff005
Vyšlo v časopise: The cohesin loader SCC2 contains a PHD finger that is required for meiosis in land plants. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008849
Kategorie: Research Article


Cohesin, a multisubunit protein complex, is required for holding sister chromatids together during mitosis and meiosis. The recruitment of cohesin by the sister chromatid cohesion 2/4 (SCC2/4) complex has been extensively studied in Saccharomyces cerevisiae mitosis, but its role in mitosis and meiosis remains poorly understood in multicellular organisms, because complete loss-of-function of either gene causes embryonic lethality. Here, we identified a weak allele of Atscc2 (Atscc2-5) that has only minor defects in vegetative development but exhibits a significant reduction in fertility. Cytological analyses of Atscc2-5 reveal multiple meiotic phenotypes including defects in chromosomal axis formation, meiosis-specific cohesin loading, homolog pairing and synapsis, and AtSPO11-1-dependent double strand break repair. Surprisingly, even though AtSCC2 interacts with AtSCC4 in vitro and in vivo, meiosis-specific knockdown of AtSCC4 expression does not cause any meiotic defect, suggesting that the SCC2-SCC4 complex has divergent roles in mitosis and meiosis. SCC2 homologs from land plants have a unique plant homeodomain (PHD) motif not found in other species. We show that the AtSCC2 PHD domain can bind to the N terminus of histones and is required for meiosis but not mitosis. Taken together, our results provide evidence that unlike SCC2 in other organisms, SCC2 requires a functional PHD domain during meiosis in land plants.

Klíčová slova:

Arabidopsis thaliana – Centromeres – Genetically modified plants – Histones – Meiosis – Mitosis – Pollen – Seeds


1. Zamariola L, Tiang CL, De Storme N, Pawlowski W, Geelen D. Chromosome segregation in plant meiosis. Front Plant Sci. 2014;5:279. Epub 2014/07/06. doi: 10.3389/fpls.2014.00279 24987397.

2. Potapova T, Gorbsky GJ. The consequences of chromosome segregation errors in mitosis and meiosis. Biology (Basel). 2017;6(1). Epub 2017/02/18. doi: 10.3390/biology6010012 28208750.

3. Makrantoni V, Marston AL. Cohesin and chromosome segregation. Curr Biol. 2018;28(12):R688–R93. Epub 2018/06/20. doi: 10.1016/j.cub.2018.05.019 29920258.

4. Haering CH, Gruber S. SnapShot: SMC protein complexes part I. Cell. 2016;164(1–2):326–e1. Epub 2016/01/16. doi: 10.1016/j.cell.2015.12.026 26771499.

5. Litwin I, Wysocki R. New insights into cohesin loading. Curr Genet. 2018;64(1):53–61. doi: 10.1007/s00294-017-0723-6 28631016

6. Li Y, Muir KW, Bowler MW, Metz J, Haering CH, Panne D. Structural basis for Scc3-dependent cohesin recruitment to chromatin. Elife. 2018;7. Epub 2018/08/16. doi: 10.7554/eLife.38356 30109982.

7. Nasmyth K, Haering CH. Cohesin: its roles and mechanisms. Annu Rev Genet. 2009;43:525–58. Epub 2009/11/06. doi: 10.1146/annurev-genet-102108-134233 19886810.

8. Liu Cm CM, McElver J, Tzafrir I, Joosen R, Wittich P, Patton D, et al. Condensin and cohesin knockouts in Arabidopsis exhibit a titan seed phenotype. Plant J. 2002;29(4):405–15. Epub 2002/02/16. doi: 10.1046/j.1365-313x.2002.01224.x 11846874.

9. Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N, Belcram K, et al. AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci. 2005;118(Pt 20):4621–32. Epub 2005/09/24. doi: 10.1242/jcs.02583 16176934.

10. Yuan L, Yang X, Ellis JL, Fisher NM, Makaroff CA. The Arabidopsis SYN3 cohesin protein is important for early meiotic events. Plant J. 2012;71(1):147–60. Epub 2012/03/03. doi: 10.1111/j.1365-313X.2012.04979.x 22381039.

11. Lam WS, Yang XH, Makaroff CA. Characterization of Arabidopsis thaliana SMC1 and SMC3: evidence that AtSMC3 may function beyond chromosome cohesion. J Cell Sci. 2005;118(14):3037–48. doi: 10.1242/jcs.02443 15972315

12. Bai X, Peirson BN, Dong F, Xue C, Makaroff CA. Isolation and characterization of SYN1, a RAD21-like gene essential for meiosis in Arabidopsis. Plant Cell. 1999;11(3):417–30. doi: 10.1105/tpc.11.3.417 10072401.

13. Dong F, Cai X, Makaroff CA. Cloning and characterization of two Arabidopsis genes that belong to the RAD21/REC8 family of chromosome cohesin proteins. Gene. 2001;271(1):99–108. doi: 10.1016/s0378-1119(01)00499-1 11410371

14. da Costa-Nunes JA, Bhatt AM, O'Shea S, West CE, Bray CM, Grossniklaus U, et al. Characterization of the three Arabidopsis thaliana RAD21 cohesins reveals differential responses to ionizing radiation. J Exp Bot. 2006;57(4):971–83. Epub 2006/02/21. doi: 10.1093/jxb/erj083 16488915.

15. Jiang L, Xia M, Strittmatter LI, Makaroff CA. The Arabidopsis cohesin protein SYN3 localizes to the nucleolus and is essential for gametogenesis. Plant J. 2007;50(6):1020–34. doi: 10.1111/j.1365-313X.2007.03106.x 17488242

16. Cai X, Dong F, Edelmann RE, Makaroff CA. The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J Cell Sci. 2003;116(Pt 14):2999–3007. Epub 2003/06/05. doi: 10.1242/jcs.00601 12783989.

17. Bhatt AM, Lister C, Page T, Fransz P, Findlay K, Jones GH, et al. The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family. Plant J. 1999;19(4):463–72. Epub 1999/10/03. doi: 10.1046/j.1365-313x.1999.00548.x 10504568.

18. Mercier R, Vezon D, Bullier E, Motamayor JC, Sellier A, Lefevre F, et al. SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes Dev. 2001;15(14):1859–71. Epub 2001/07/19. doi: 10.1101/gad.203201 11459834.

19. De K, Sterle L, Krueger L, Yang X, Makaroff CA. Arabidopsis thaliana WAPL is essential for the prophase removal of cohesin during meiosis. PLoS Genet. 2014;10(7):e1004497. Epub 2014/07/18. doi: 10.1371/journal.pgen.1004497 25033056.

20. Yang C, Hamamura Y, Sofroni K, Böwer F, Stolze SC, Nakagami H, et al. SWITCH 1/DYAD is a WINGS APART-LIKE antagonist that maintains sister chromatid cohesion in meiosis. Nat Commun. 2019;10(1):1755. doi: 10.1038/s41467-019-09759-w 30988453

21. Bolanos-Villegas P, De K, Pradillo M, Liu D, Makaroff CA. In favor of establishment: regulation of chromatid cohesion in plants. Front Plant Sci. 2017;8:846. Epub 2017/06/08. doi: 10.3389/fpls.2017.00846 28588601.

22. Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Shevchenko A, et al. Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell. 2000;5(2):243–54. Epub 2000/07/06. doi: 10.1016/s1097-2765(00)80420-7 10882066.

23. Kogut I, Wang J, Guacci V, Mistry RK, Megee PC. The Scc2/Scc4 cohesin loader determines the distribution of cohesin on budding yeast chromosomes. Genes Dev. 2009;23(19):2345–57. Epub 2009/10/03. doi: 10.1101/gad.1819409 19797771.

24. Bermudez VP, Farina A, Higashi TL, Du F, Tappin I, Takahashi TS, et al. In vitro loading of human cohesin on DNA by the human Scc2-Scc4 loader complex. Proc Natl Acad Sci U S A. 2012;109(24):9366–71. Epub 2012/05/26. doi: 10.1073/pnas.1206840109 22628566.

25. Watrin E, Schleiffer A, Tanaka K, Eisenhaber F, Nasmyth K, Peters JM. Human Scc4 is required for cohesin binding to chromatin, sister-chromatid cohesion, and mitotic progression. Curr Biol. 2006;16(9):863–74. Epub 2006/05/10. doi: 10.1016/j.cub.2006.03.049 16682347.

26. Chao WC, Murayama Y, Munoz S, Costa A, Uhlmann F, Singleton MR. Structural studies reveal the functional modularity of the Scc2-Scc4 cohesin loader. Cell Rep. 2015;12(5):719–25. Epub 2015/07/28. doi: 10.1016/j.celrep.2015.06.071 26212329.

27. Minina EA, Reza SH, Gutierrez-Beltran E, Elander PH, Bozhkov PV, Moschou PN. The Arabidopsis homolog of Scc4/MAU2 is essential for embryogenesis. J Cell Sci. 2017;130(6):1051–63. Epub 2017/02/01. doi: 10.1242/jcs.196865 28137757.

28. Hinshaw SM, Makrantoni V, Kerr A, Marston AL, Harrison SC. Structural evidence for Scc4-dependent localization of cohesin loading. Elife. 2015;4:e06057. Epub 2015/06/04. doi: 10.7554/eLife.06057 26038942.

29. Hinshaw SM, Makrantoni V, Harrison SC, Marston AL. The kinetochore receptor for the cohesin loading complex. Cell. 2017;171(1):72–84.e13. Epub 2017/09/25. doi: 10.1016/j.cell.2017.08.017 28938124.

30. Murayama Y, Uhlmann F. Biochemical reconstitution of topological DNA binding by the cohesin ring. Nature. 2014;505(7483):367–71. Epub 2013/12/03. doi: 10.1038/nature12867 24291789.

31. Petela NJ, Gligoris TG, Metson J, Lee BG, Voulgaris M, Hu B, et al. Scc2 is a potent activator of cohesin's ATPase that promotes loading by binding Scc1 without Pds5. Mol Cell. 2018;70(6):1134-+. doi: 10.1016/j.molcel.2018.05.022 29932904

32. Takahashi TS, Yiu P, Chou MF, Gygi S, Walter JC. Recruitment of Xenopus Scc2 and cohesin to chromatin requires the pre-replication complex. Nat Cell Biol. 2004;6(10):991–6. Epub 2004/09/28. doi: 10.1038/ncb1177 15448702.

33. Takahashi TS, Basu A, Bermudez V, Hurwitz J, Walter JC. Cdc7-Drf1 kinase links chromosome cohesion to the initiation of DNA replication in Xenopus egg extracts. Genes Dev. 2008;22(14):1894–905. Epub 2008/07/17. doi: 10.1101/gad.1683308 18628396.

34. Zheng G, Kanchwala M, Xing C, Yu H. MCM2-7-dependent cohesin loading during S phase promotes sister-chromatid cohesion. Elife. 2018;7. Epub 2018/04/04. doi: 10.7554/eLife.33920 29611806.

35. He Y, Wang J, Qi W, Song R. Maize Dek15 encodes the cohesin-loading complex subunit SCC4 and is essential for chromosome segregation and kernel development. Plant Cell. 2019. Epub 2019/02/02. doi: 10.1105/tpc.18.00921 30705131.

36. Sebastian J, Ravi M, Andreuzza S, Panoli AP, Marimuthu MP, Siddiqi I. The plant adherin AtSCC2 is required for embryogenesis and sister-chromatid cohesion during meiosis in Arabidopsis. Plant J. 2009;59(1):1–13. Epub 2009/02/21. doi: 10.1111/j.1365-313X.2009.03845.x 19228337.

37. Neuffer MG, Sheridan WF. Defective kernel mutants of maize. I. Genetic and lethality studies. Genetics. 1980;95(4):929–44. Epub 1980/08/01. 17249053.

38. Kurosaki T, Popp MW, Maquat LE. Quality and quantity control of gene expression by nonsense-mediated mRNA decay. Nat Rev Mol Cell Biol. 2019;20(7):406–20. Epub 2019/04/18. doi: 10.1038/s41580-019-0126-2 30992545.

39. Tanaka T, Fuchs J, Loidl J, Nasmyth K. Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation. Nat Cell Biol. 2000;2(8):492–9. Epub 2000/08/10. doi: 10.1038/35019529 10934469.

40. Yu H, Wang M, Tang D, Wang K, Chen F, Gong Z, et al. OsSPO11-1 is essential for both homologous chromosome pairing and crossover formation in rice. Chromosoma. 2010;119(6):625–36. Epub 2010/07/14. doi: 10.1007/s00412-010-0284-7 20625906.

41. Turinetto V, Giachino C. Multiple facets of histone variant H2AX: a DNA double-strand-break marker with several biological functions. Nucleic Acids Res. 2015;43(5):2489–98. Epub 2015/02/26. doi: 10.1093/nar/gkv061 25712102.

42. Kurzbauer MT, Uanschou C, Chen D, Schlogelhofer P. The recombinases DMC1 and RAD51 are functionally and spatially separated during meiosis in Arabidopsis. Plant Cell. 2012;24(5):2058–70. Epub 2012/05/17. doi: 10.1105/tpc.112.098459 22589466.

43. Lightfoot J, Testori S, Barroso C, Martinez-Perez E. Loading of meiotic cohesin by SCC-2 is required for early processing of DSBs and for the DNA damage checkpoint. Curr Biol. 2011;21(17):1421–30. Epub 2011/08/23. doi: 10.1016/j.cub.2011.07.007 21856158.

44. Grelon M, Vezon D, Gendrot G, Pelletier G. AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J. 2001;20(3):589–600. doi: 10.1093/emboj/20.3.589 11157765.

45. Mercier R, Armstrong SJ, Horlow C, Jackson NP, Makaroff CA, Vezon D, et al. The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. Development. 2003;130(14):3309–18. doi: 10.1242/dev.00550 12783800

46. Higgins JD, Armstrong SJ, Franklin FCH, Jones GH. The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev. 2004;18(20):2557–70. doi: 10.1101/gad.317504 15489296

47. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP. The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genet. 2007;3(8):e132. doi: 10.1371/journal.pgen.0030132 17696612.

48. Armstrong SJ, Caryl AP, Jones GH, Franklin FC. Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci. 2002;115(Pt 18):3645–55. doi: 10.1242/jcs.00048 12186950.

49. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH. The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Gene Dev. 2005;19(20):2488–500. doi: 10.1101/gad.354705 16230536

50. Ku J-C, Ronceret A, Golubovskaya I, Lee DH, Wang C, Timofejeva L, et al. Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis. PLoS Genet. 2020;16(4):e1007881. doi: 10.1371/journal.pgen.1007881 32310948

51. Sanchez R, Zhou MM. The PHD finger: a versatile epigenome reader. Trends Biochem Sci. 2011;36(7):364–72. doi: 10.1016/j.tibs.2011.03.005 21514168

52. Lee WY, Lee D, Chung WI, Kwon CS. Arabidopsis ING and Alfin1-like protein families localize to the nucleus and bind to H3K4me3/2 via plant homeodomain fingers. Plant J. 2009;58(3):511–24. Epub 2009/01/22. doi: 10.1111/j.1365-313X.2009.03795.x 19154204.

53. Lan F, Collins RE, De Cegli R, Alpatov R, Horton JR, Shi X, et al. Recognition of unmethylated histone H3 lysine 4 links BHC80 to LSD1-mediated gene repression. Nature. 2007;448(7154):718–22. Epub 2007/08/10. doi: 10.1038/nature06034 17687328.

54. Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018;46(W1):W296–W303. Epub 2018/05/23. doi: 10.1093/nar/gky427 29788355.

55. Kikuchi S, Borek DM, Otwinowski Z, Tomchick DR, Yu H. Crystal structure of the cohesin loader Scc2 and insight into cohesinopathy. Proc Natl Acad Sci U S A. 2016;113(44):12444–9. Epub 2016/11/03. doi: 10.1073/pnas.1611333113 27791135.

56. Chao WC, Murayama Y, Munoz S, Jones AW, Wade BO, Purkiss AG, et al. Structure of the cohesin loader Scc2. Nat Commun. 2017;8:13952. Epub 2017/01/07. doi: 10.1038/ncomms13952 28059076.

57. Heidinger-Pauli JM, Mert O, Davenport C, Guacci V, Koshland D. Systematic reduction of cohesin differentially affects chromosome segregation, condensation, and DNA Repair. Curr Biol. 2010;20(10):957–63. doi: 10.1016/j.cub.2010.04.018 20451387

58. Mellor J. It takes a PHD to read the histone code. Cell. 2006;126(1):22–4. doi: 10.1016/j.cell.2006.06.028 16839870

59. Andreuzza S, Nishal B, Singh A, Siddiqi I. The chromatin protein DUET/MMD1 controls expression of the meiotic gene TDM1 during male meiosis in Arabidopsis. PLoS Genet. 2015;11(9).

60. Wang J, Niu BX, Huang JY, Wang HK, Yang XH, Dong AW, et al. The PHD finger protein MMD1/DUET ensures the progression of male meiotic chromosome condensation and directly regulates the expression of the condensin gene CAP-D3. Plant Cell. 2016;28(8):1894–909. doi: 10.1105/tpc.16.00040 27385818

61. Delwiche CF, Cooper ED. The evolutionary origin of a terrestrial flora. Curr Biol. 2015;25(19):R899–910. Epub 2015/10/07. doi: 10.1016/j.cub.2015.08.029 26439353.

62. Loidl J. Conservation and variability of meiosis across the eukaryotes. Annu Rev Genet. 2016;50:293–316. Epub 2016/10/01. doi: 10.1146/annurev-genet-120215-035100 27686280.

63. Niklas KJ, Cobb ED, Kutschera U. Did meiosis evolve before sex and the evolution of eukaryotic life cycles? Bioessays. 2014;36(11):1091–101. doi: 10.1002/bies.201400045 25143284

64. Gao D, Zhu B, Cao X, Zhang M, Wang X. Roles of NIPBL in maintenance of genome stability. Semin Cell Dev Biol. 2019;90:181–6. Epub 2018/08/11. doi: 10.1016/j.semcdb.2018.08.005 30096364.

65. Gillespie PJ, Hirano T. Scc2 couples replication licensing to sister chromatid cohesion in Xenopus egg extracts. Curr Biol. 2004;14(17):1598–603. Epub 2004/09/03. doi: 10.1016/j.cub.2004.07.053 15341749.

66. Huang J, Hsu JM, Laurent BC. The RSC nucleosome-remodeling complex is required for Cohesin's association with chromosome arms. Mol Cell. 2004;13(5):739–50. doi: 10.1016/s1097-2765(04)00103-0 15023343

67. Francis KE, Lam SY, Harrison BD, Bey AL, Berchowitz LE, Copenhaver GP. Pollen tetrad-based visual assay for meiotic recombination in Arabidopsis. Proc Natl Acad Sci U S A. 2007;104(10):3913–8. Epub 2007/03/16. doi: 10.1073/pnas.0608936104 17360452.

68. Garcia Valérie B H, Camescasse Delphine, Granier Fabienne, Bouchez David, Tissier Alain. AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell. 2003;15(1):119–32. doi: 10.1105/tpc.006577 12509526

69. Li WX, Chen CB, Markmann-Mulisch U, Timofejeva L, Schmelzer E, Ma H, et al. The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. P Natl Acad Sci USA. 2004;101(29):10596–601. doi: 10.1073/pnas.0404110101 15249667

70. Hartung F, Suer S, Bergmann T, Puchta H. The role of AtMUS81 in DNA repair and its genetic interaction with the helicase AtRecQ4A. Nucleic Acids Res. 2006;34(16):4438–48. Epub 2006/09/02. doi: 10.1093/nar/gkl576 16945961.

71. Schubert V, Weissleder A, Ali H, Fuchs J, Lermontova I, Meister A, et al. Cohesin gene defects may impair sister chromatid alignment and genome stability in Arabidopsis thaliana. Chromosoma. 2009;118(5):591–605. doi: 10.1007/s00412-009-0220-x 19533160

72. Sun Y, Ambrose JH, Haughey BS, Webster TD, Pierrie SN, Munoz DF, et al. Deep genome-wide measurement of meiotic gene conversion using tetrad analysis in Arabidopsis thaliana. PLoS Genet. 2012;8(10):e1002968. Epub 2012/10/12. doi: 10.1371/journal.pgen.1002968 23055940.

73. Yang S, Yuan Y, Wang L, Li J, Wang W, Liu H, et al. Great majority of recombination events in Arabidopsis are gene conversion events. Proc Natl Acad Sci U S A. 2012;109(51):20992–7. Epub 2012/12/06. doi: 10.1073/pnas.1211827110 23213238.

74. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. Epub 2014/04/04. doi: 10.1093/bioinformatics/btu170 24695404.

75. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, et al. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 2012;40(Database issue):D1202–10. Epub 2011/12/06. doi: 10.1093/nar/gkr1090 22140109.

76. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754–60. Epub 2009/05/20. doi: 10.1093/bioinformatics/btp324 19451168.

77. Qi J, Zhao F, Buboltz A, Schuster SC. inGAP: an integrated next-generation genome analysis pipeline. Bioinformatics. 2010;26(1):127–9. Epub 2009/11/03. doi: 10.1093/bioinformatics/btp615 19880367.

78. Qi J, Zhao F. inGAP-sv: a novel scheme to identify and visualize structural variation from paired end mapping data. Nucleic Acids Res. 2011;39(Web Server issue):W567–75. Epub 2011/07/08. doi: 10.1093/nar/gkr506 21715388.

79. Qi J, Chen Y, Copenhaver GP, Ma H. Detection of genomic variations and DNA polymorphisms and impact on analysis of meiotic recombination and genetic mapping. Proc Natl Acad Sci U S A. 2014;111(27):10007–12. Epub 2014/06/25. doi: 10.1073/pnas.1321897111 24958856.

80. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–8. Epub 2002/02/16. doi: 10.1006/meth.2001.1262 11846609.

81. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 2005;139(1):5–17. Epub 2005/09/17. doi: 10.1104/pp.105.063743 16166256.

82. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16(6):735–43. doi: 10.1046/j.1365-313x.1998.00343.x 10069079.

83. Peterson R, Slovin PJ, Chen C. A simplified method for differential staining of aborted and non-aborted pollen grains. Int J Plant Biol. 2010;1.

84. Wang Y, Cheng Z, Lu P, Timofejeva L, Ma H. Molecular cell biology of male meiotic chromosomes and isolation of male meiocytes in Arabidopsis thaliana. In: Riechmann JL, Wellmer F, editors. Flower Development: Methods and Protocols. New York, NY: Springer New York; 2014. p. 217–30.

85. Wang Y, Cheng Z, Huang J, Shi Q, Hong Y, Copenhaver GP, et al. The DNA replication factor RFC1 is required for interference-sensitive meiotic crossovers in Arabidopsis thaliana. PLoS Genet. 2012;8(11):e1003039. Epub 2012/11/13. doi: 10.1371/journal.pgen.1003039 23144629.

86. Wang C, Huang J, Zhang J, Wang H, Han Y, Copenhaver GP, et al. The largest subunit of DNA polymerase delta is required for normal formation of meiotic type I crossovers. Plant Physiol. 2018. doi: 10.1104/pp.18.00861 30459265.

87. Ren R, Wang H, Guo C, Zhang N, Zeng L, Chen Y, et al. Widespread whole genome duplications contribute to genome complexity and species diversity in Angiosperms. Mol Plant. 2018;11(3):414–28. Epub 2018/01/11. doi: 10.1016/j.molp.2018.01.002 29317285.

88. Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M, et al. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat Commun. 2014;5:3978. Epub 2014/05/29. doi: 10.1038/ncomms4978 24865297.

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