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Conspecific pollen advantage mediated by the extragynoecial compitum and its potential to resist interspecific reproductive interference between two Sagittaria species

The extragynoecial compitum formed by the incomplete fusion of carpel margins, while allowing intercarpellary growth of pollen tubes in apocarpous angiosperms, may also increase the risk of reproductive interference caused by heterospecific pollen (HP) deposition. In Sagittaria, congeneric HP tubes...

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Autores principales: Fei, Cai-Hong, Tang, Sha-Sha, Shang, Shu-He, Dai, Jie, Wang, Xin-Yi, Wang, Shuai, Liu, Wei-Qi, Wang, Xiao-Fan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9354020/
https://www.ncbi.nlm.nih.gov/pubmed/35937372
http://dx.doi.org/10.3389/fpls.2022.956193
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author Fei, Cai-Hong
Tang, Sha-Sha
Shang, Shu-He
Dai, Jie
Wang, Xin-Yi
Wang, Shuai
Liu, Wei-Qi
Wang, Xiao-Fan
author_facet Fei, Cai-Hong
Tang, Sha-Sha
Shang, Shu-He
Dai, Jie
Wang, Xin-Yi
Wang, Shuai
Liu, Wei-Qi
Wang, Xiao-Fan
author_sort Fei, Cai-Hong
collection PubMed
description The extragynoecial compitum formed by the incomplete fusion of carpel margins, while allowing intercarpellary growth of pollen tubes in apocarpous angiosperms, may also increase the risk of reproductive interference caused by heterospecific pollen (HP) deposition. In Sagittaria, congeneric HP tubes grow via different paths and enter the ovules later than conspecific pollen (CP) tubes. However, it is unclear how the growth advantage of the CP tube helps ensure reproductive success when HP is deposited on the stigmas. We performed molecular characterization of interspecies-pollinated seeds to examine the consequences of interspecific pollen deposition between Sagittaria pygmaea and S. trifolia. We also conducted CP–HP (1:1) mixed pollination and delayed CP pollination treatments to explore the seed-siring abilities of CP and HP. Our results showed that although HP could trigger the development of fruits, the interspecies-pollinated seeds contained partially developed embryos and could not germinate. More than 70% of the embryos in these seeds were molecularly identified as hybrids of both species, suggesting that HP tubes could enter the ovules and fertilize the egg cells. Moreover, CP could sire more offspring (≥70%) after the CP–HP (1:1) mixed pollination treatment, even when HP reached the stigma 0.5–1 h earlier than CP (≥50%). Following adequate CP vs. HP (1:1) pollination on carpels on two sides of the apocarpous gynoecium, both species produced > 70% conspecific seeds, indicating that the CP tubes could occupy ovules that should be occupied by HP via the extragynoecial compitum. Our results reveal that in Sagittaria, pollen deposition from co-existing congeneric heterospecies leads to interspecific seed discounting. However, the CP advantage mediated by the extragynoecial compitum is an effective strategy to mitigate the effects of interspecific pollen deposition. This study improves our understanding of how apocarpous angiosperms with an extragynoecial compitum can maintain species stability and mitigate the negative reproductive interference effect from sympatrically distributed related species.
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spelling pubmed-93540202022-08-06 Conspecific pollen advantage mediated by the extragynoecial compitum and its potential to resist interspecific reproductive interference between two Sagittaria species Fei, Cai-Hong Tang, Sha-Sha Shang, Shu-He Dai, Jie Wang, Xin-Yi Wang, Shuai Liu, Wei-Qi Wang, Xiao-Fan Front Plant Sci Plant Science The extragynoecial compitum formed by the incomplete fusion of carpel margins, while allowing intercarpellary growth of pollen tubes in apocarpous angiosperms, may also increase the risk of reproductive interference caused by heterospecific pollen (HP) deposition. In Sagittaria, congeneric HP tubes grow via different paths and enter the ovules later than conspecific pollen (CP) tubes. However, it is unclear how the growth advantage of the CP tube helps ensure reproductive success when HP is deposited on the stigmas. We performed molecular characterization of interspecies-pollinated seeds to examine the consequences of interspecific pollen deposition between Sagittaria pygmaea and S. trifolia. We also conducted CP–HP (1:1) mixed pollination and delayed CP pollination treatments to explore the seed-siring abilities of CP and HP. Our results showed that although HP could trigger the development of fruits, the interspecies-pollinated seeds contained partially developed embryos and could not germinate. More than 70% of the embryos in these seeds were molecularly identified as hybrids of both species, suggesting that HP tubes could enter the ovules and fertilize the egg cells. Moreover, CP could sire more offspring (≥70%) after the CP–HP (1:1) mixed pollination treatment, even when HP reached the stigma 0.5–1 h earlier than CP (≥50%). Following adequate CP vs. HP (1:1) pollination on carpels on two sides of the apocarpous gynoecium, both species produced > 70% conspecific seeds, indicating that the CP tubes could occupy ovules that should be occupied by HP via the extragynoecial compitum. Our results reveal that in Sagittaria, pollen deposition from co-existing congeneric heterospecies leads to interspecific seed discounting. However, the CP advantage mediated by the extragynoecial compitum is an effective strategy to mitigate the effects of interspecific pollen deposition. This study improves our understanding of how apocarpous angiosperms with an extragynoecial compitum can maintain species stability and mitigate the negative reproductive interference effect from sympatrically distributed related species. Frontiers Media S.A. 2022-07-22 /pmc/articles/PMC9354020/ /pubmed/35937372 http://dx.doi.org/10.3389/fpls.2022.956193 Text en Copyright © 2022 Fei, Tang, Shang, Dai, Wang, Wang, Liu and Wang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Fei, Cai-Hong
Tang, Sha-Sha
Shang, Shu-He
Dai, Jie
Wang, Xin-Yi
Wang, Shuai
Liu, Wei-Qi
Wang, Xiao-Fan
Conspecific pollen advantage mediated by the extragynoecial compitum and its potential to resist interspecific reproductive interference between two Sagittaria species
title Conspecific pollen advantage mediated by the extragynoecial compitum and its potential to resist interspecific reproductive interference between two Sagittaria species
title_full Conspecific pollen advantage mediated by the extragynoecial compitum and its potential to resist interspecific reproductive interference between two Sagittaria species
title_fullStr Conspecific pollen advantage mediated by the extragynoecial compitum and its potential to resist interspecific reproductive interference between two Sagittaria species
title_full_unstemmed Conspecific pollen advantage mediated by the extragynoecial compitum and its potential to resist interspecific reproductive interference between two Sagittaria species
title_short Conspecific pollen advantage mediated by the extragynoecial compitum and its potential to resist interspecific reproductive interference between two Sagittaria species
title_sort conspecific pollen advantage mediated by the extragynoecial compitum and its potential to resist interspecific reproductive interference between two sagittaria species
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9354020/
https://www.ncbi.nlm.nih.gov/pubmed/35937372
http://dx.doi.org/10.3389/fpls.2022.956193
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