ATP depletion plays a pivotal role in self‐incompatibility, revealing a link between cellular energy status, cytosolic acidification and actin remodelling in pollen tubes

Ludi Wang; Zongcheng Lin; Jose Carli; Agnieszka Gladala-Kostarz; Julia Davies; Vernonica Franklin-Tong; Maurice Bosch

doi:10.1111/nph.18350

ATP depletion plays a pivotal role in self‐incompatibility, revealing a link between cellular energy status, cytosolic acidification and actin remodelling in pollen tubes

Ludi Wang, Zongcheng Lin, Jose Carli, Agnieszka Gladala-Kostarz, Julia Davies, Vernonica Franklin-Tong^*, Maurice Bosch^*

^*Corresponding author for this work

Biosciences

Research output: Contribution to journal › Article › peer-review

Abstract

Self-incompatibility (SI) involves specific interactions during pollination to reject incompatible (‘self’) pollen, preventing inbreeding in angiosperms. A key event observed in pollen undergoing the Papaver rhoeas SI response is the formation of punctate F-actin foci.

Pollen tube growth is heavily energy-dependent, yet ATP levels in pollen tubes have not been directly measured during SI. Here we used transgenic Arabidopsis lines expressing the Papaver pollen S-determinant to investigate a possible link between ATP levels, cytosolic pH ([pH]cyt) and alterations to the actin cytoskeleton.

We identify for the first time that SI triggers a rapid and significant ATP depletion in pollen tubes. Artificial depletion of ATP triggered cytosolic acidification and formation of actin aggregates. We also identify in vivo, evidence for a threshold [pH]cyt of 5.8 for actin foci formation. Imaging revealed that SI stimulates acidic cytosolic patches adjacent to the plasma membrane.

In conclusion, this study provides evidence that ATP depletion plays a pivotal role in SI upstream of programmed cell death and reveals a link between the cellular energy status, cytosolic acidification and alterations to the actin cytoskeleton in regulating Papaver SI in pollen tubes.

Original language	English
Pages (from-to)	1691-1707
Journal	New Phytologist
Volume	236
Issue number	5
Early online date	1 Jul 2022
DOIs	https://doi.org/10.1111/nph.18350
Publication status	Published - Dec 2022

Bibliographical note

Biotechnology and Biological Sciences Research Council. Grant Numbers: BB/P005489/1, BB/T00486X/1

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@article{46fd0c58d9e349ee9f3b735635e9f192,

title = "ATP depletion plays a pivotal role in self‐incompatibility, revealing a link between cellular energy status, cytosolic acidification and actin remodelling in pollen tubes",

abstract = "Self-incompatibility (SI) involves specific interactions during pollination to reject incompatible ({\textquoteleft}self{\textquoteright}) pollen, preventing inbreeding in angiosperms. A key event observed in pollen undergoing the Papaver rhoeas SI response is the formation of punctate F-actin foci.Pollen tube growth is heavily energy-dependent, yet ATP levels in pollen tubes have not been directly measured during SI. Here we used transgenic Arabidopsis lines expressing the Papaver pollen S-determinant to investigate a possible link between ATP levels, cytosolic pH ([pH]cyt) and alterations to the actin cytoskeleton.We identify for the first time that SI triggers a rapid and significant ATP depletion in pollen tubes. Artificial depletion of ATP triggered cytosolic acidification and formation of actin aggregates. We also identify in vivo, evidence for a threshold [pH]cyt of 5.8 for actin foci formation. Imaging revealed that SI stimulates acidic cytosolic patches adjacent to the plasma membrane.In conclusion, this study provides evidence that ATP depletion plays a pivotal role in SI upstream of programmed cell death and reveals a link between the cellular energy status, cytosolic acidification and alterations to the actin cytoskeleton in regulating Papaver SI in pollen tubes.",

author = "Ludi Wang and Zongcheng Lin and Jose Carli and Agnieszka Gladala-Kostarz and Julia Davies and Vernonica Franklin-Tong and Maurice Bosch",

note = "Biotechnology and Biological Sciences Research Council. Grant Numbers: BB/P005489/1, BB/T00486X/1",

year = "2022",

month = dec,

doi = "10.1111/nph.18350",

language = "English",

volume = "236",

pages = "1691--1707",

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T1 - ATP depletion plays a pivotal role in self‐incompatibility, revealing a link between cellular energy status, cytosolic acidification and actin remodelling in pollen tubes

AU - Wang, Ludi

AU - Lin, Zongcheng

AU - Carli, Jose

AU - Gladala-Kostarz, Agnieszka

AU - Davies, Julia

AU - Franklin-Tong, Vernonica

AU - Bosch, Maurice

N1 - Biotechnology and Biological Sciences Research Council. Grant Numbers: BB/P005489/1, BB/T00486X/1

PY - 2022/12

Y1 - 2022/12

N2 - Self-incompatibility (SI) involves specific interactions during pollination to reject incompatible (‘self’) pollen, preventing inbreeding in angiosperms. A key event observed in pollen undergoing the Papaver rhoeas SI response is the formation of punctate F-actin foci.Pollen tube growth is heavily energy-dependent, yet ATP levels in pollen tubes have not been directly measured during SI. Here we used transgenic Arabidopsis lines expressing the Papaver pollen S-determinant to investigate a possible link between ATP levels, cytosolic pH ([pH]cyt) and alterations to the actin cytoskeleton.We identify for the first time that SI triggers a rapid and significant ATP depletion in pollen tubes. Artificial depletion of ATP triggered cytosolic acidification and formation of actin aggregates. We also identify in vivo, evidence for a threshold [pH]cyt of 5.8 for actin foci formation. Imaging revealed that SI stimulates acidic cytosolic patches adjacent to the plasma membrane.In conclusion, this study provides evidence that ATP depletion plays a pivotal role in SI upstream of programmed cell death and reveals a link between the cellular energy status, cytosolic acidification and alterations to the actin cytoskeleton in regulating Papaver SI in pollen tubes.

AB - Self-incompatibility (SI) involves specific interactions during pollination to reject incompatible (‘self’) pollen, preventing inbreeding in angiosperms. A key event observed in pollen undergoing the Papaver rhoeas SI response is the formation of punctate F-actin foci.Pollen tube growth is heavily energy-dependent, yet ATP levels in pollen tubes have not been directly measured during SI. Here we used transgenic Arabidopsis lines expressing the Papaver pollen S-determinant to investigate a possible link between ATP levels, cytosolic pH ([pH]cyt) and alterations to the actin cytoskeleton.We identify for the first time that SI triggers a rapid and significant ATP depletion in pollen tubes. Artificial depletion of ATP triggered cytosolic acidification and formation of actin aggregates. We also identify in vivo, evidence for a threshold [pH]cyt of 5.8 for actin foci formation. Imaging revealed that SI stimulates acidic cytosolic patches adjacent to the plasma membrane.In conclusion, this study provides evidence that ATP depletion plays a pivotal role in SI upstream of programmed cell death and reveals a link between the cellular energy status, cytosolic acidification and alterations to the actin cytoskeleton in regulating Papaver SI in pollen tubes.

U2 - 10.1111/nph.18350

DO - 10.1111/nph.18350

M3 - Article

SN - 0028-646X

VL - 236

SP - 1691

EP - 1707

JO - New Phytologist

JF - New Phytologist

IS - 5

ER -

ATP depletion plays a pivotal role in self‐incompatibility, revealing a link between cellular energy status, cytosolic acidification and actin remodelling in pollen tubes

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