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精子来源的父系效应对根干细胞生态位分化的影响。

Sperm-origin paternal effects on root stem cell niche differentiation.

机构信息

State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China.

State Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, China.

出版信息

Nature. 2024 Oct;634(8032):220-227. doi: 10.1038/s41586-024-07885-0. Epub 2024 Aug 28.

DOI:10.1038/s41586-024-07885-0
PMID:39198649
Abstract

Fertilization introduces parental genetic information into the zygote to guide embryogenesis. Parental contributions to postfertilization development have been discussed for decades, and the data available show that both parents contribute to the zygotic transcriptome, suggesting a paternal role in early embryogenesis. However, because the specific paternal effects on postfertilization development and the molecular pathways underpinning these effects remain poorly understood, paternal contribution to early embryogenesis and plant development has not yet been adequately demonstrated. Here our research shows that TREE1 and its homologue DAZ3 are expressed exclusively in Arabidopsis sperm. Despite presenting no evident defects in sperm development and fertilization, tree1 daz3 unexpectedly led to aberrant differentiation of the embryo root stem cell niche. This defect persisted in seedlings and disrupted root tip regeneration, comparable to congenital defects in animals. TREE1 and DAZ3 function by suppression of maternal RKD2 transcription, thus mitigating the detrimental maternal effects from RKD2 on root stem cell niche. Therefore, our findings illuminate how genetic deficiencies in sperm can exert enduring paternal effects on specific plant organ differentiation and how parental-of-origin genes interact to ensure normal embryogenesis. This work also provides a new concept of how gamete quality or genetic deficiency can affect specific plant organ formation.

摘要

受精将父母的遗传信息引入受精卵,指导胚胎发生。几十年来,人们一直在讨论父母对受精后发育的贡献,现有数据表明,父母双方都为受精卵转录组做出了贡献,这表明父亲在早期胚胎发生中有一定作用。然而,由于具体的父本对受精后发育的影响以及支持这些影响的分子途径仍知之甚少,因此,父本对早期胚胎发生和植物发育的贡献尚未得到充分证明。在这里,我们的研究表明,TREE1 和其同源物 DAZ3 仅在拟南芥精子中表达。尽管在精子发育和受精过程中没有明显缺陷,但 tree1 daz3 出人意料地导致胚胎根干细胞龛的异常分化。该缺陷在幼苗中持续存在,并破坏根尖再生,与动物的先天性缺陷相当。TREE1 和 DAZ3 通过抑制母体 RKD2 的转录来发挥作用,从而减轻 RKD2 对根干细胞龛的不利母体效应。因此,我们的研究结果阐明了精子中的遗传缺陷如何对特定植物器官的分化产生持久的父本效应,以及亲本来源的基因如何相互作用以确保正常的胚胎发生。这项工作还提供了一个新概念,即配子质量或遗传缺陷如何影响特定植物器官的形成。

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Sperm-origin paternal effects on root stem cell niche differentiation.精子来源的父系效应对根干细胞生态位分化的影响。
Nature. 2024 Oct;634(8032):220-227. doi: 10.1038/s41586-024-07885-0. Epub 2024 Aug 28.
2
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本文引用的文献

1
EGG CELL 1 contributes to egg-cell-dependent preferential fertilization in Arabidopsis.卵母细胞 1 有助于拟南芥中依赖卵母细胞的优先受精。
Nat Plants. 2024 Feb;10(2):268-282. doi: 10.1038/s41477-023-01616-5. Epub 2024 Jan 29.
2
Spatially expressed WIP genes control Arabidopsis embryonic root development.空间表达的 WIP 基因控制拟南芥胚胎根发育。
Nat Plants. 2022 Jun;8(6):635-645. doi: 10.1038/s41477-022-01172-4. Epub 2022 Jun 16.
3
H3K27 methylation regulates the fate of two cell lineages in male gametophytes.H3K27 甲基化调控雄性配子体中两个细胞谱系的命运。
Plant Cell. 2022 Jul 30;34(8):2989-3005. doi: 10.1093/plcell/koac136.
4
The parental contributions to early plant embryogenesis and the concept of maternal-to-zygotic transition in plants.双亲对子代植物胚胎发生的贡献和植物中母体到合子转变的概念。
Curr Opin Plant Biol. 2022 Feb;65:102144. doi: 10.1016/j.pbi.2021.102144. Epub 2021 Nov 22.
5
Differential impact of four sperm preparation techniques on sperm motility, morphology, DNA fragmentation, acrosome status, oxidative stress, and mitochondrial activity: A prospective study.四种精子制备技术对精子活力、形态、DNA 碎片、顶体状态、氧化应激和线粒体活性的影响差异:一项前瞻性研究。
Andrology. 2021 Sep;9(5):1549-1559. doi: 10.1111/andr.13038. Epub 2021 Jun 18.
6
The E3 ligase MREL57 modulates microtubule stability and stomatal closure in response to ABA.E3 连接酶 MREL57 通过调节微管稳定性和 ABA 响应下的气孔关闭。
Nat Commun. 2021 Apr 12;12(1):2181. doi: 10.1038/s41467-021-22455-y.
7
Fertilized egg cells secrete endopeptidases to avoid polytubey.受精卵分泌内肽酶以避免多管。
Nature. 2021 Apr;592(7854):433-437. doi: 10.1038/s41586-021-03387-5. Epub 2021 Mar 31.
8
Plant egg cell fate determination depends on its exact position in female gametophyte.植物卵细胞命运的决定取决于其在雌配子体中的精确位置。
Proc Natl Acad Sci U S A. 2021 Feb 23;118(8). doi: 10.1073/pnas.2017488118.
9
TREE1-EIN3-mediated transcriptional repression inhibits shoot growth in response to ethylene.TREE1-EIN3 介导的转录抑制响应乙烯抑制茎生长。
Proc Natl Acad Sci U S A. 2020 Nov 17;117(46):29178-29189. doi: 10.1073/pnas.2018735117. Epub 2020 Nov 2.
10
Equal parental contribution to the transcriptome is not equal control of embryogenesis.父母双方对等的转录组贡献并不等于胚胎发生的对等控制。
Nat Plants. 2020 Nov;6(11):1354-1364. doi: 10.1038/s41477-020-00793-x. Epub 2020 Oct 26.