Cytological mechanism of pollen abortion induced by high temperature in Populus canescens
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摘要:目的 研究高温处理对银灰杨小孢子发生的影响，揭示高温处理导致杨树花粉败育的细胞学机理，旨在完善高温处理诱导配子染色体加倍、选育林木三倍体的技术。方法 本研究以银灰杨为试验材料，利用38 ℃和41 ℃的高温，对不同减数分裂时期的银灰杨花粉母细胞进行3、6 h处理，研究处理温度、减数分裂时期以及持续处理时间对败育花粉比率的影响。在此基础上，通过比较未经高温处理和高温处理后银灰杨花粉母细胞减数分裂染色体行为、微管骨架动态变化以及减数后绒毡层细胞发育的差异，揭示高温处理诱导银灰杨花粉败育的细胞学机理。结果 （1）减数分裂时期、处理温度、持续处理时间以及减数分裂时期与处理温度、减数分裂时期与持续处理时间的交互作用均对败育花粉比率具有极显著的影响。41 ℃高温于中期Ⅰ持续处理3 h的败育花粉比率最高，为（25.11 ± 4.28）%。（2）与对照组相比，银灰杨雄花芽经高温处理后，花粉母细胞减数分裂微管骨架表现出不同程度的解聚，中期Ⅰ和中期Ⅱ的部分纺锤体微管缺失，致使后期Ⅰ和后期Ⅱ的同源染色体或姊妹染色单体分离异常，产生大量的落后染色体。这些落后染色体被遗弃在细胞质中，引起微核的产生，四分体时期形成多分体而导致花粉败育。（3）高温处理可导致银灰杨花药绒毡层退化延迟，但仍能正常开裂，释放出花粉粒，因此绒毡层延迟退化不是高温处理诱导银灰杨花粉败育的原因。结论 高温处理诱导银灰杨花粉母细胞中期Ⅰ和中期Ⅱ的部分纺锤体微管缺失，致使后期Ⅰ和后期Ⅱ产生大量的落后染色体，引起大量多分体的产生，是高温处理诱导银灰杨花粉败育的细胞学机理。Abstract:Objective The effects of high temperature on microsporogenisis and cytological mechanism of pollen abortion induced by high temperature were conducted in P. canescens, aiming at improving the technology of forest triploid breeding though inducing gamete chromosme doubling by high temperature.Method In this study, the effects of high temperature, meiotic stage and duration on percentage of aborted pollen were conducted after male flower buds being exposed to 38 ℃ for 3 or 6 h in P. canescens. Subsequently, the differences in chromosome behaviour, meiotic microtubule cytoskeleton and development of tapetum between untreated pollen mother cells (PMCs) and treated PMCs were studied to reveal the cytological mechanism of aborted pollen production induced by high temperature.Result (1) Meiotic stages, temperature, duration, meiotic stage × temperature interactions and meiotic stage × duration interactions had significant effects on percentage of aborted pollen. The highest percentage of aborted pollen was (25.11 ± 4.28)% when PMCs were treated with 41 ℃ for 3 h at metaphase Ⅰ. (2) Compared with PMCs in the control group, meiotic microtubule cytoskeleton was depolymerized and some spindles were lost within the PMCs at metaphase Ⅰ and Ⅱ, leading to the abnormal chromosome segregation at anaphase Ⅰ and Ⅱ and forming a great number of lagging chromosomes. These lagging chromosomes were retained within cytoplasm, causing some micronuclei to form. Therefore, aborted pollen formed due to the formation of polyads at tetrad stage. (3) Although high temperature could also delay the degradation of the tapetum, the anthers normally dehisced and pollen grains were released. Thus, the delayed degradation of the tapetum was not responsible for the formation of aborted pollen.Conclusion After male flower buds being treated by 38 ℃ for 3 or 6 h, some spindles are lost within the PMCs at metaphase Ⅰ and Ⅱ, leading to form a great number of lagging chromosomes and polyads, which is the cytological mechanism of aborted pollen formation induced by high temperature.
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Keywords:
- Populus canescens /
- high temperature /
- aborted pollen /
- meiosis /
- microtubule cytoskeleton /
- tapetum
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图 1 银灰杨高温处理组（a）和对照组（b）的败育花粉
黑色箭头指向的为败育花粉。The black arrow shows aborted pollen.
Figure 1. Aborted pollen in the treatment (a) and control group (b) of P. canescens
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图 2 银灰杨花粉母细胞对照组和38 ℃高温处理组的染色体行为
a. 对照组后期Ⅰ；b. 对照组后期Ⅱ；c. 对照组的四分体；d. 38 ℃高温持续处理3 h后期Ⅰ的落后染色体；e. 38 ℃高温持续处理3 h后期Ⅱ的落后染色体；f. 38 ℃高温持续处理3 h后四分体时期产生的多分体；g. 38 ℃高温持续处理6 h后期Ⅰ的落后染色体；h. 38 ℃高温持续处理6 h后期Ⅱ的落后染色体；i. 38 ℃高温持续处理6 h后四分体时期产生的多分体。黑色箭头指向的为落后染色体。标尺为10.0 μm。a, anaphase Ⅰ in control group; b, lagging chromosomes at anaphase Ⅱ in control group; c, normal tetrad in control group; d, lagging chromosomes in anaphase Ⅰ derived from the treatment under 38 ℃ for 3 h; e, lagging chromosomes in anaphase Ⅱ derived from the treatment under 38 ℃ for 3 h; f, polyad derived from the treatment under 38 ℃ for 3 h; g, lagging chromosomes in anaphase Ⅰ derived from the treatment under 38 ℃ for 6 h; h, lagging chromosomes in anaphase Ⅱ derived from the treatment under 38 ℃ for 6 h; I, polyad derived from the treatment under 38 ℃ for 6 h. The black arrow shows the lagging chromosomes. Bar = 10.0 μm.
Figure 2. Meiotic chromosome behaviours of PMCs in the control group and the treated groups under 38 ℃ high temperature in P. canescens
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图 3 银灰杨花粉母细胞对照组38 ℃高温处理组的微管骨架
a. 对照组中期Ⅰ；b. 对照组后期Ⅰ；c. 对照组中期Ⅱ；d. 对照组后期Ⅱ；e. 对照组末期Ⅱ；f. 处理组（38 ℃高温处理3 h）的中期Ⅰ；g. 处理组（38 ℃高温处理3 h）的后期Ⅰ；h. 处理组（38 ℃高温处理3 h）的中期Ⅱ；i. 处理组（38 ℃高温处理3 h）的后期Ⅱ；j. 处理组（38 ℃高温处理3 h）的末期Ⅱ；k. 处理组（38 ℃高温处理6 h）中期Ⅰ；l. 处理组（38 ℃高温处理6 h）的后期Ⅰ；m. 处理组（38 ℃高温处理6 h）的中期Ⅱ；n. 处理组（38 ℃高温处理6 h）的后期Ⅱ；o. 处理组（38℃高温处理6 h）的末期Ⅱ。标尺为10.0 μm。a, metaphase Ⅰ in the control group; b, anaphase Ⅰ in the control group; c, metaphase Ⅱ in the control group; d, anaphase Ⅱ in the control group; e, telophase Ⅱ in the control group; f, metaphase Ⅰ in the treatment group under 38 ℃ for 3 h; g, anaphase Ⅰ in the treatment group under 38 ℃ for 3 h; h, metaphase Ⅱ in the treatment group under 38 ℃ for 3 h; i, anahase Ⅱ in the treatment group under 38 ℃ for 3 h; j, telophase Ⅱ in the treatment group under 38 ℃ for 3 h; k, metaphase Ⅰ in the treatment group under 38 ℃ for 6 h; l, anaphase Ⅰ in the treatment group under 38 ℃ for 6 h; m, metahase Ⅱ in the treatment group under 38 ℃ for 6 h; n, anahase Ⅱ in the treatment group under 38 ℃ for 6 h; o, telophase Ⅱ in the treatment group under 38 ℃ for 6 h. Scalebar = 10.0 μm.
Figure 3. Meiotic microtubular cytoskeletons of PMCs in the control group and the treated groups under 38 ℃ in P. canescens
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图 4 银灰杨对照组和38 ℃高温处理组的花药绒毡层发育进程
a. 对照组四分体时期；b. 对照组四分体形成后2 d；c. 对照组四分体形成后4 d；d. 对照组四分体形成后6 d；e. 对照组四分体形成后8 d；f. 38 ℃的高温持续处理3 h后四分体时期；g. 38 ℃的高温持续处理3 h，四分体形成后2 d；h. 38 ℃的高温持续处理3 h，四分体形成后4 d；i. 38 ℃的高温持续处理3 h四分体形成后6 d； j. 38 ℃的高温持续处理3 h，四分体形成后8 d；k. 38 ℃的高温持续处理6 h后四分体时期；l. 38 ℃的高温持续处理6 h，四分体形成后2 d； m. 38 ℃的高温持续处理6 h，四分体形成后4 d；n. 38 ℃的高温持续处理6 h，四分体形成后6 d； o. 38 ℃的高温持续处理6 h，四分体形成后8 d。黑色箭头指向的为绒毡层。标尺为5.0 μm。a, tapetum of anthers from the control group at the tetrad stage. b, tapetum of anthers from the control group 2 d after the tetrad stage. c, tapetum of anthers from the control group 4 d after the tetrad stage. d, tapetum of anthers from the control group 6 d after the tetrad stage. e, tapetum of anthers from the control group 8 d after the tetrad stage. f, tapetum of anthers in the treatment under 38 ℃ for 3 h at the tetrad stage. g, tapetum of anthers in the treatment under 38 ℃ for 3 h, 2 d after the tetrad stage. h, tapetum of anthers in the treatment under 38 ℃ for 3 h, 4 d after the tetrad stage. i, tapetum of anthers in the treatment under 38 ℃ for 3 h, 6 d after the tetrad stage. j, tapetum of anthers in the treatment under 38 ℃ for 3 h, 8 d after the tetrad stage. k, tapetum of anthers in the treatment under 38 ℃ for 6 h at the tetrad stage. l, tapetum of anthers in the treatment under 38 ℃ for 6 h, 2 d after the tetrad stage. m, tapetum of anthers in the treatment under 38 ℃ for 6 h, 4 d after the tetrad stage. n, tapetum of anthers in the treatment under 38 ℃ for 6 h, 6 d after the tetrad stage. o, tapetum of anthers in the treatment under 38 ℃ for 6 h, 8 d after the tetrad stage. The black arrow points to the tapetum. Scale bar = 5.0 μm.
Figure 4. Tapetum development process of anthers in the control group and the treated groups under 38 ℃ high temperature in P. canescens
表 1 不同高温处理组合的败育花粉比率
Table 1 Percentage of aborted pollen derived from different high temperature treatment combinations of P. canescens
减数分裂时期
Meiotic stage处理温度
Treating
temperature/℃持续处理时间
Continuous treating time/h败育花粉比率
Percentage of
aborted pollen/%细线期
Leptotene38 3 9.45 ± 0.92 6 17.15 ± 2.56 41 3 11.29 ± 1.77 6 17.92 ± 2.55 偶线期
Zygotene38 3 12.78 ± 5.06 6 22.45 ± 2.21 41 3 17.39 ± 5.65 6 20.37 ± 0.83 粗线期
Pachytene38 3 15.72 ± 2.02 6 15.35 ± 4.33 41 3 18.61 ± 5.20 6 16.16 ± 1.35 双线期
Diplotene38 3 19.90 ± 3.03 6 19.33 ± 0.96 41 3 20.97 ± 4.10 6 20.93 ± 1.70 终变期
Diakinesis38 3 14.17 ± 1.80 6 13.83 ± 1.73 41 3 16.95 ± 1.82 6 20.62 ± 3.49 中期Ⅰ
Metaphase Ⅰ38 3 10.82 ± 3.41 6 13.76 ± 2.06 41 3 25.11 ± 4.28 6 24.13 ± 4.05 对照 Control 7.58 ± 1.32 注：对照组为不进行高温处理的雄花芽。下同。Notes: the control group consists of male flower buds that are not subjected to high temperature treatment. The same below. 
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表 2 38 ℃处理3 h与6 h后出现落后染色体的花粉母细胞比率
Table 2 Percentage of lagging chromosomes treated under38 ℃ for 3 and 6 h
持续处理时间
Continuous treating time/h落后染色体的花粉母细胞比率
Percentage of PMCs with lagging chromosome/%后期Ⅰ Anaphase Ⅰ 后期Ⅱ Anaphase Ⅱ 3 40.67 ± 3.06 b 33.33 ± 8.00 b 6 55.33 ± 4.16 b 48.67 ± 3.06 b 对照 Control 22.67 ± 4.16 a 13.33 ± 5.03 a 注：不同小写字母表示在0.05水平上显著。Note: different lowercase letters represent significance at 0.05 level.
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