The lipid flippases ALA4 and ALA5 play critical roles in cell expansion and plant growth

Jeffrey A. Davis, Randall B. Pares, Tilde Bernstein, Stephen C. McDowell, Elizabeth Brown, Jason Stubrich, Alexa Rosenberg, Edgar B. Cahoon, Rebecca E. Cahoon, Lisbeth R. Poulsen, Michael Palmgren, Rosa L. López-Marqués, Jeffrey F. Harper

Research output: Contribution to journalArticle

2 Scopus citations

Abstract

Aminophospholipid ATPases (ALAs) are lipid flippases involved in transporting specific lipids across membrane bilayers. Arabidopsis (Arabidopsis thaliana) contains 12 ALAs in five phylogenetic clusters, including four in cluster 3 (ALA4-ALA7). ALA4/5 and ALA6/7, are expressed primarily in vegetative tissues and pollen, respectively. Previously, a double knockout of ALA6/7 was shown to result in pollen fertility defects. Here we show that a double knockout of ALA4/5 results in dwarfism, characterized by reduced growth in rosettes (6.5-fold), roots (4.3-fold), bolts (4.5-fold), and hypocotyls (2-fold). Reduced cell size was observed for multiple vegetative cell types, suggesting a role for ALA4/5 in cellular expansion. Members of the third ALA cluster are at least partially interchangeable, as transgenes expressing ALA6 in vegetative tissues partially rescued ala4/5 mutant phenotypes, and expression of ALA4 transgenes in pollen fully rescued ala6/7 mutant fertility defects. ALA4-GFP displayed plasma membrane and endomembrane localization patterns when imaged in both guard cells and pollen. Lipid profiling revealed ala4/5 rosettes had perturbations in glycerolipid and sphingolipid content. Assays in yeast revealed that ALA5 can flip a variety of glycerolipids and the sphingolipid sphingomyelin across membranes. These results support a model whereby the flippase activity of ALA4 and ALA5 impacts the homeostasis of both glycerolipids and sphingolipids and is important for cellular expansion during vegetative growth.

Original languageEnglish (US)
Pages (from-to)2111-2125
Number of pages15
JournalPlant physiology
Volume182
Issue number4
DOIs
StatePublished - Apr 2020

ASJC Scopus subject areas

  • Physiology
  • Genetics
  • Plant Science

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    Davis, J. A., Pares, R. B., Bernstein, T., McDowell, S. C., Brown, E., Stubrich, J., Rosenberg, A., Cahoon, E. B., Cahoon, R. E., Poulsen, L. R., Palmgren, M., López-Marqués, R. L., & Harper, J. F. (2020). The lipid flippases ALA4 and ALA5 play critical roles in cell expansion and plant growth. Plant physiology, 182(4), 2111-2125. https://doi.org/10.1104/PP.19.01332