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 E. Franklin-Tong, Maurice Bosch

Research output: Contribution to journalArticlepeer-review

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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 languageEnglish
Pages (from-to)1691-1707
Number of pages17
JournalNew Phytologist
Volume236
Issue number5
Early online date23 Jul 2022
DOIs
Publication statusPublished - 03 Nov 2022

Keywords

  • actin cytoskeleton
  • Arabidopsis
  • ATP
  • cytosolic acidification
  • Papaver rhoeas
  • pH
  • pollen tubes
  • self-incompatibility

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