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胼胝质缺乏调节水稻花粉母细胞和绒毡层细胞中胞间连丝的频率和细胞外距离。

Callose deficiency modulates plasmodesmata frequency and extracellular distance in rice pollen mother and tapetal cells.

作者信息

Somashekar Harsha, Takanami Keiko, Benitez-Alfonso Yoselin, Oishi Akane, Hiratsuka Rie, Nonomura Ken-Ichi

机构信息

Plant Cytogenetics Laboratory, National Institute of Genetics, Mishima, Japan.

School of Life Science, The Graduate University for Advanced Studies, SOKENDAI, Hayama, Kanagawa, Japan.

出版信息

Ann Bot. 2024 Dec 31;134(6):1013-1026. doi: 10.1093/aob/mcae137.

DOI:10.1093/aob/mcae137
PMID:39140870
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC11687631/
Abstract

BACKGROUND AND AIMS

Fertilization relies on pollen mother cells able to transition from mitosis to meiosis to supply gametes. This process involves remarkable changes at the molecular, cellular and physiological levels, including (but not limited to) remodelling of the cell wall. During the onset of meiosis, the cellulose content in the pollen mother cell walls gradually declines, with the concurrent deposition of the polysaccharide callose in anther locules. We aim to understand the biological significance of cellulose-to-callose turnover in pollen mother cells walls.

METHODS

We carried out electron microscopic, aniline blue and renaissance staining analyses of rice flowers.

KEY RESULTS

Our observations indicate that in wild-type rice anthers, the mitosis-to-meiosis transition coincides with a gradual reduction in the number of cytoplasmic connections called plasmodesmata. A mutant in the Oryza sativa callose synthase GSL5 (Osgsl5-3), impaired in callose accumulation in premeiotic and meiotic anthers, displayed a greater reduction in plasmodesmata frequency among pollen mother cells and tapetal cells, suggesting a role for callose in maintenance of plasmodesmata. In addition, a significant increase in extracellular distance between pollen mother cells and impaired premeiotic cell shaping was observed in the Osgsl5-3 mutant.

CONCLUSIONS

The results suggest that callose-to-cellulose turnover during the transition from mitosis to meiosis is necessary to maintain cell-to-cell connections and optimal extracellular distance among the central anther locular cells. The findings of this study contribute to our understanding of the regulatory influence of callose metabolism during initiation of meiosis in flowering plants.

摘要

背景与目的

受精依赖于能够从有丝分裂转变为减数分裂以提供配子的花粉母细胞。这一过程涉及分子、细胞和生理水平上的显著变化,包括(但不限于)细胞壁的重塑。在减数分裂开始时,花粉母细胞壁中的纤维素含量逐渐下降,同时多糖胼胝质在花药室中沉积。我们旨在了解花粉母细胞壁中纤维素向胼胝质转变的生物学意义。

方法

我们对水稻花进行了电子显微镜、苯胺蓝和复兴染色分析。

关键结果

我们的观察表明,在野生型水稻花药中,有丝分裂向减数分裂的转变与称为胞间连丝的细胞质连接数量逐渐减少相吻合。水稻胼胝质合成酶GSL5(Osgsl5 - 3)的一个突变体,在减数分裂前和减数分裂期花药中的胼胝质积累受损,花粉母细胞和绒毡层细胞之间的胞间连丝频率有更大程度的降低,表明胼胝质在维持胞间连丝方面发挥作用。此外,在Osgsl5 - 3突变体中观察到花粉母细胞之间的细胞外距离显著增加以及减数分裂前细胞形态受损。

结论

结果表明,从有丝分裂到减数分裂转变过程中胼胝质向纤维素的转变对于维持花药中央室细胞之间的细胞间连接和最佳细胞外距离是必要的。本研究结果有助于我们理解开花植物减数分裂起始过程中胼胝质代谢的调控影响。

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本文引用的文献

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Impact of protein domains on the MEL2 granule, a cytoplasmic ribonucleoprotein complex maintaining faithful meiosis progression in rice.蛋白质结构域对 MEL2 颗粒的影响,MEL2 颗粒是一种细胞质核糖核蛋白复合物,可维持水稻中减数分裂的保真度。
New Phytol. 2024 Sep;243(6):2235-2250. doi: 10.1111/nph.19968. Epub 2024 Jul 24.
2
Plasmodesmata: Channels Under Pressure.质膜通道:压力下的通道
Annu Rev Plant Biol. 2024 Jul;75(1):291-317. doi: 10.1146/annurev-arplant-070623-093110. Epub 2024 Jul 2.
3
The transcription factors and pathways underpinning male reproductive development in Arabidopsis.支撑拟南芥雄性生殖发育的转录因子和信号通路。
Front Plant Sci. 2024 Feb 8;15:1354418. doi: 10.3389/fpls.2024.1354418. eCollection 2024.
4
Genetic Regulation of Mitosis-Meiosis Fate Decision in Plants: Is Callose an Oversighted Polysaccharide in These Processes?植物有丝分裂-减数分裂命运决定的遗传调控:胼胝质在这些过程中是一种被忽视的多糖吗?
Plants (Basel). 2023 May 9;12(10):1936. doi: 10.3390/plants12101936.
5
Intercellular Communication during Stomatal Development with a Focus on the Role of Symplastic Connection.细胞间通讯在气孔发育中的作用,重点关注胞间连丝的作用。
Int J Mol Sci. 2023 Jan 30;24(3):2593. doi: 10.3390/ijms24032593.
6
Rice GLUCAN SYNTHASE-LIKE5 promotes anther callose deposition to maintain meiosis initiation and progression.水稻葡聚糖合酶 LIKE5 促进花粉粒胼胝质沉积以维持减数分裂起始和进程。
Plant Physiol. 2023 Jan 2;191(1):400-413. doi: 10.1093/plphys/kiac488.
7
Mechanics of Pollen Tube Elongation: A Perspective.花粉管伸长的机制:一种观点
Front Plant Sci. 2020 Oct 20;11:589712. doi: 10.3389/fpls.2020.589712. eCollection 2020.
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Interplay between turgor pressure and plasmodesmata during plant development.植物发育过程中膨压与胞间连丝的相互作用。
J Exp Bot. 2020 Jan 23;71(3):768-777. doi: 10.1093/jxb/erz434.
9
Interactions between callose and cellulose revealed through the analysis of biopolymer mixtures.通过分析生物聚合物混合物揭示的胼胝质和纤维素之间的相互作用。
Nat Commun. 2018 Oct 31;9(1):4538. doi: 10.1038/s41467-018-06820-y.
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Plasmodesmata at a glance.质膜通道结构域速览。
J Cell Sci. 2018 Jun 7;131(11):jcs209346. doi: 10.1242/jcs.209346.