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A Flow Cytometry-Based Analysis to Establish a Cell Cycle www.nature.com/scientificreports OPEN A fow cytometry-based analysis to establish a cell cycle synchronization protocol for Saccharum spp. Shan Yang 1,5, Kai Zeng1,5, Ling Luo1, Wang Qian1, Zhiqiang Wang2, Jaroslav Doležel 3, Muqing Zhang 2, Xiangxiong Gao4 & Zuhu Deng1,2* Modern sugarcane is an unusually complex heteroploid crop, and its genome comprises two or three subgenomes. To reduce the complexity of sugarcane genome research, the ploidy level and number of chromosomes can be reduced using fow chromosome sorting. However, a cell cycle synchronization (CCS) protocol for Saccharum spp. is needed that maximizes the accumulation of metaphase chromosomes. For fow cytometry analysis in this study, we optimized the lysis bufer, hydroxyurea(HU) concentration, HU treatment time and recovery time for sugarcane. We determined the mitotic index by microscopic observation and calculation. We found that WPB bufer was superior to other bufers for preparation of sugarcane nuclei suspensions. The optimal HU treatment was 2 mM for 18 h at 25 °C, 28 °C and 30 °C. Higher recovery treatment temperatures were associated with shorter recovery times (3.5 h, 2.5 h and 1.5 h at 25 °C, 28 °C and 30 °C, respectively). The optimal conditions for treatment with the inhibitor of microtubule polymerization, amiprophos-methyl (APM), were 2.5 μM for 3 h at 25 °C, 28 °C and 30 °C. Meanwhile, preliminary screening of CCS protocols for Badila were used for some main species of genus Saccharum at 25 °C, 28 °C and 30 °C, which showed that the average mitotic index decreased from 25 °C to 30 °C. The optimal sugarcane CCS protocol that yielded a mitotic index of >50% in sugarcane root tips was: 2 mM HU for 18 h, 0.1 X Hoagland’s Solution without HU for 3.5 h, and 2.5 μM APM for 3.0 h at 25 °C. The CCS protocol defned in this study should accelerate the development of genomic research and cytobiology research in sugarcane. Sugarcane (Saccharum spp.), belonging to the genus Saccharum, is an economically valuable crop. Te genus Saccharum is diverse in genome content and organization and comprises two wild species (S. robustum and S. spontaneum) and four groups of former cultivated clones (S. ofcinarum, S. sinense, S. bareri and S. edule)1. S. ofcinarum is thought to have evolved from S. robustum2. Te genome of modern sugarcane contains 100–130 chromosomes, of which 80–90% are from S. ofcinarum and 10–20% are from S. spontaneum3. Tus, sugarcane has an unusually complex, highly polyploid and aneuploid genome that complicates analyses of genome sequence and assembly. Although genome sequencing on the tetra- ploid S. spontaneum has been performed, the assembly accuracy was not high and many gene sequences were absent4. To reduce this complexity, the sugarcane genome can be dissected into single chromosomes using fow cytometry. Since this approach requires sufcient numbers of metaphase chromosomes, a stable and efcient cell cycle synchronization (CCS) method for sugarcane is needed. Te eukaryotic cell cycle is typically divided into four phases: G1 phase, in which the cell grows and dupli- cates organelles; S phase, in which DNA synthesis occurs; G2 phase, in which the cell prepares to divide afer replication; M phase, during which the chromosomes precisely separate and form two daughter nuclei along the mitotic spindle, and cytokinesis when the actual cell division occurs5–7. Cells in each of these cell cycle phases have a distinct nuclear DNA content, which can be exploited for sorting by fow cytometry8. Furthermore, cell 1National Engineering Research Center for Sugarcane, Fujian Agriculture and Forestry University, Fuzhou, 350002, China. 2State Key Laboratory for Protection and Utilization of Subtropical Agro-Bioresources, Guangxi University, Nanning, 530004, China. 3Centre of Plant Structural and Functional Genomics, Institute of Experimental Botany, Olomouc, CZ-78371, Czech Republic. 4College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou, 350002, China. 5These authors contributed equally: Shan Yang and Kai Zeng. *email: [email protected] SCIENTIFIC REPORTS | (2020) 10:5016 | https://doi.org/10.1038/s41598-020-62086-9 1 www.nature.com/scientificreports/ www.nature.com/scientificreports No. Species Name 1 Saccharum ofcinarum 14NG124 2 Saccharum ofcinarum 51NG-103 3 Saccharum ofcinarum Badila 4 Saccharum ofcinarum Guan A 5 Saccharum ofcinarum LA Purple 6 Saccharum spontaneum 12–165 7 Saccharum spontaneum 2007–11 8 Saccharum spontaneum 87–20 9 Saccharum spontaneum Laos-2 10 Saccharum spontaneum SES-208 11 Saccharum spontaneum 82–63 12 Saccharum spontaneum 82–110 13 Saccharum spontaneum 82–114 14 Saccharum robustum 51NG3 15 Saccharum robustum 51NG63 16 Saccharum robustum 51NG155 17 Saccharum robustum NG77–004 18 Saccharum robustum 57NG208 19 Saccharum sinense Songxizhe 20 Saccharum barberi Nagans 21 Saccharum barberi Pansahi 22 Saccharum hybrid ROC22 23 Saccharum hybrid Guitang30 24 Saccharum hybrid Mintang01–77 25 Saccharum hybrid Yuetang96–86 26 Saccharum hybrid Yunzhe0551 27 Saccharum hybrid ROC10 28 Saccharum hybrid Funong40 Table 1. Saccharum species used in this study. synchronization followed by fow cytometry can be used to enrich large populations of cells in a given phase9,10. For plants in particular, isolation of metaphase chromosomes is essential for cytogenetic, cytobiologic and genomic studies11–13, yet cells in this phase represent only 5–10% of the total cell population. Moreover, cell cycle progression in plant tissues proceeds asynchronously14. Artifcial CCS is a prerequisite for obtaining high concentrations of chromosomes. Stable synchronization schemes for various plants have been established using actively growing cell cultures or root tips15,16. In contrast to cell culture, plant root tips are a good source of chromosomes and are also cheaper, more stable and easier to handle17. As such, increasing numbers of researchers are using plant root tips as starting materials for CCS stud- ies. To date, there are two main CCS strategies: (i) collection of specifc cell populations using physical methods such as centrifugal elutriation9; and (ii) treatment of cells with chemical inhibitors that impede DNA synthe- sis inhibitors or microtubule polymerization as well as other metaphase blocking chemicals15. CCS in root tips from several crops, including cereal, wheat, Chinese fr and Vicia faba can be achieved with chemical inhibitors 17–20. Moreover, DNA synthesis inhibitors such as hydroxyurea (HU), deoxyadenosine and deoxythymidine, and microtubule inhibitors such as trifuralin and amiprophos-methyl (APM), are efective for CCS in plant root tips8. DNA synthesis inhibitors and microtubule inhibitors together can also be more efective to achieve CCS than either agent alone13,18. Te timing of the mitotic cycle of diferent plant species varies according to genome size. Terefore, given the complexity of the sugarcane genome and the variety of clones, developing a stable CCS method has been challenging. Based on results obtained for predecessors in other crops, in this study we examined the efect of treatment temperature, chemical inhibitor concentration and processing time. We analyzed diferent chemical inhibitor concentrations and processing times for Badila (S. ofcinarum, 2n = 8 × =80) roots at diferent temper- atures by fow cytometry and microscopy to compile preliminary CCS protocols, which we then screened using diferent temperatures and diferent Saccharum clones. Finally, we defned a stable and optimal CCS protocol for sugarcane, which could greatly promote the development of sugarcane cytology and genomics. Material and methods Plant material. In this study, 5 S. officinarum clones, 8 S. spontaneum clones, 5 S. robustum clones, 1 Saccharum sinense clone, 2 S. barberi clones and 7 Saccharum hybrid clones were used for CCS (Table 1). All clones were obtained from the Fujian Agricultural and Forestry University sugarcane germplasm resources nurs- ery (Fuzhou, China) and were cut into single bud stems. Tese single bud stems were cleaned, soaked in 0.5% SCIENTIFIC REPORTS | (2020) 10:5016 | https://doi.org/10.1038/s41598-020-62086-9 2 www.nature.com/scientificreports/ www.nature.com/scientificreports Bufer Composition References 15 mM Tris; 2 mM Na EDTA·2H O; 0.5 mM spermine·4HCl; 80 mM KCl; 20 mM NaCl; 15 mM LB01 2 2 15 HOCH2CH2SH; 0.1% (v/v) Triton X-100; pH 7.5 9.53 mM MgSO ·7H O; 47.67 mM KCl; 4.77 mM HEPES; 6.48 mM DTT; 0.25% (v/v) Triton MgSO 4 2 36 4 X-100; pH 8.0 0.2 M Tris·HCl; 4 mM MgCl ·6H O; 2 mM Na EDTA·2H O; 86 mM NaCl; 10 mM Na S O ; 1% WPB 2 2 2 2 2 2 5 23 PVP-10; 1%(v/v) Triton X-100; pH 7.5 0.5 mM spermine·4HCl; 30 mM Na C H O ·2H O; 20 mM MOPS; 80 mM KCl; 20 mM NaCl; 0.5% GPB 3 6 5 7 2 23 (v/v) Triton X-100; pH 7.0 200 mM mannitol; 10 mM MOPS; 0.05% (v/v) Triton X-100; 10 mM KCl; 10 mM NaCl; 2.5 mM Bino’s 37 DTT; 10 mM spermine·4HCl; 2.5 mM Na2EDTA·2H2O; 0.05% (w/v) sodium azide; pH 5.8 Otto I: 100 mM C H O ·H O; 0.5% (v/v) Tween 20; pH approx. 2–3 Otto II: 400 mM Otto’s 6 8 7 2 38 Na2PO4·12H2O; pH approx. 8–9 10 mM Tris; 10 mM Na EDTA; 100 mM NaCl; 0.1% Triton X-100; 2% formaldehyde stock Formaldehyde fxative 2 16 solution(37%, v/v); pH 7.5 15 Tris bufer 10 mM Tris; 10 mM Na2EDTA; 100 mM NaCl; pH 9 Table 2. Bufers used in this study. carbendazim solution for 24 h, placed in a pallet and covered with perlite, kept moist with ddH2O and incubated in the dark at 25 ± 0.5 °C, 28 ± 0.5 °C or 30 ± 0.5 °C in a biological incubator.
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