Fertilized egg cells secrete endopeptidases to avoid polytubey

Yu, Xiaobo; Zhang, Xuecheng; Zhao, Peng; Peng, Xiongbo; Chen, Hong; Bleckmann, Andrea; Bazhenova, A.F.; Shi, Ce; Dresselhaus, Thomas; Sun, Mingwei

doi:10.1038/s41586-021-03387-5

Cited by 57 publications

(58 citation statements)

References 40 publications

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“…Taken together, we have shown that ECS1 and ECS2 regulate offspring genome size via haploid and polyspermy induction. In addition, our observation of evident single fertilization and a temporal delay of second synergid disintegration provides an alternative explanation for the attraction of supernumerary pollen tubes observed both by Yu et al 1 . and in this study.…”

supporting

confidence: 64%

“…This safeguard mechanism is only activated after successful fertilization of both female gametes and involves the disintegration of pollen tube attracting synergid cells. Yu and coworkers previously reported that the endopeptidase ECS1 and ECS2, which are secreted by fertilized egg cells, prevent the attraction of supernumerary pollen tubes by cleaving the pollen tube attractant LURE1 1 . Here we report on an earlier defect in ecs1 ecs2 mutants that is manifested by single rather than double fertilization of either egg or central cell.…”

mentioning

confidence: 99%

“…Yu et al 1 investigated two aspartic endopeptidases, ECS1 and ECS2, that are secreted from the egg cell towards the filiform apparatus upon sperm-egg fusion. In addition, they provide a compelling set of evidence demonstrating that both ECS1 and ECS2 can cleave specific variants of LURE1.…”

mentioning

confidence: 99%

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ECS1 and ECS2 regulate polyspermy and suppress the formation of haploid plants by promoting double fertilization

Mao

Nakel

Serbes

et al. 2022

Preprint

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In flowering plants, the number of pollen tubes that provide sperm cells to the female gametes is restricted by a pollen tube block. This safeguard mechanism is only activated after successful fertilization of both female gametes and involves the disintegration of pollen tube attracting synergid cells. Yu and coworkers previously reported that the endopeptidase ECS1 and ECS2, which are secreted by fertilized egg cells, prevent the attraction of supernumerary pollen tubes by cleaving the pollen tube attractant LURE11. Here we report on an earlier defect in ecs1 ecs2 mutants that is manifested by single rather than double fertilization of either egg or central cell. The defect is accompanied by a delay in synergid disintegration providing an alternative explanation for the extra pollen tubes observed in the double mutant. These results are corroborated by our finding that ecs1 ecs2 plants segregate both, haploid plants and plants resulting from polyspermy.

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supporting

confidence: 64%

mentioning

confidence: 99%

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ECS1 and ECS2 regulate polyspermy and suppress the formation of haploid plants by promoting double fertilization

Mao

Nakel

Serbes

et al. 2022

Preprint

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“…Finally, four members of the EGG CELL‐SPECIFIC ( ECS ) gene family encoding eukaryotic A1 aspartic endopeptidases were strongly upregulated in the P. patens egg cell (Table S7). Two members of this family ( AtECS1 and AtECS2 ) are exclusively expressed in the Arabidopsis egg from which they are secreted to the extracellular space after fertilization to prevent polytubey (Sprunck et al ., 2012; Yu et al ., 2021).…”

Section: Resultsmentioning

confidence: 99%

The Physcomitrium patens egg cell expresses several distinct epigenetic components and utilizes homologues of BONOBO genes for cell specification

et al. 2022

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Summary Although land plant germ cells have received much attention, knowledge about their specification is still limited. We thus identified transcripts enriched in egg cells of the bryophyte model species Physcomitrium patens, compared the results with angiosperm egg cells, and selected important candidate genes for functional analysis. We used laser‐assisted microdissection to perform a cell‐type‐specific transcriptome analysis on egg cells for comparison with available expression profiles of vegetative tissues and male reproductive organs. We made reporter lines and knockout mutants of the two BONOBO (PbBNB) genes and studied their role in reproduction. We observed an overlap in gene activity between bryophyte and angiosperm egg cells, but also clear differences. Strikingly, several processes that are male‐germline specific in Arabidopsis are active in the P. patens egg cell. Among those were the moss PbBNB genes, which control proliferation and identity of both female and male germlines. Pathways shared between male and female germlines were most likely present in the common ancestors of land plants, besides sex‐specifying factors. A set of genes may also be involved in the switches between the diploid and haploid moss generations. Nonangiosperm gene networks also contribute to the specification of the P. patens egg cell.

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“…Synergid disintegration and the establishment of a pollen tube block is a multiphasic process. It involves (i) fertilization-induced cleavage of LURE1 by the egg-secreted endopeptidases ECS1 and ECS2 ( Yu et al., 2021 ), (ii) dilution of LURE by fusion of the synergid with the central cell in a process that requires central cell fertilization ( Maruyama et al., 2015 ), and (iii) synergid nucleus disintegration ( Völz et al., 2013 ; Maruyama et al., 2015 ). The last step is regulated by fertilization-independent seed–Polycomb Repressive Complex 2 as well as the transcription factors EIN3 and EIL1, which are components of the ethylene response pathway ( Maruyama et al., 2013 , 2015 ; Völz et al., 2013 ).…”

Section: Introductionmentioning

confidence: 99%

Dual and opposing roles of EIN3 reveal a generation conflict during seed growth

Heydlauff

Serbes

et al. 2022

Molecular Plant

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Seed size critically affects grain yield of crops and hence represents a key breeding target. The development of embryo-nourishing endosperm is a key driver of seed expansion. We here report unexpected dual roles of the transcription factor EIN3 in regulating seed size. These EIN3 functions have remained largely undiscovered because they oppose each other. Capitalizing on the analysis of multiple ethylene biosynthesis mutants, we demonstrate that EIN3 represses endosperm and seed development in a pathway regulated by ethylene. We, in addition, provide evidence that EIN3-mediated synergid nucleus disintegration promotes endosperm expansion. Interestingly, synergid nucleus disintegration is not affected in various ethylene biosynthesis mutants, suggesting that this promoting function of EIN3 is independent of ethylene. Whereas the growth-inhibitory ethylene-dependent EIN3 action appears to be encoded by sporophytic tissue, the growth-promoting role of EIN3 is induced by fertilization, revealing a generation conflict that converges toward the key signaling component EIN3.

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Fertilized egg cells secrete endopeptidases to avoid polytubey

Cited by 57 publications

References 40 publications

ECS1 and ECS2 regulate polyspermy and suppress the formation of haploid plants by promoting double fertilization

ECS1 and ECS2 regulate polyspermy and suppress the formation of haploid plants by promoting double fertilization

The Physcomitrium patens egg cell expresses several distinct epigenetic components and utilizes homologues of BONOBO genes for cell specification

Dual and opposing roles of EIN3 reveal a generation conflict during seed growth

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