Halotropism requires phospholipase Dζ1‐mediated modulation of cellular polarity of auxin transport carriers

Abstract

Endocytosis and relocalization of auxin carriers represent important mechanisms for adaptive plant growth and developmental responses. Both root gravitropism and halotropism have been shown to be dependent on relocalization of auxin transporters. Following their homology to mammalian phospholipase Ds (PLDs), plant PLDζ‐type enzymes are likely candidates to regulate auxin carrier endocytosis. We investigated root tropic responses for an Arabidopsis pldζ1‐KO mutant and its effect on the dynamics of two auxin transporters during salt stress, that is, PIN2 and AUX1. We found altered root growth and halotropic and gravitropic responses in the absence of PLDζ1 and report a role for PLDζ1 in the polar localization of PIN2. Additionally, irrespective of the genetic background, salt stress induced changes in AUX1 polarity. Utilizing our previous computational model, we found that these novel salt‐induced AUX1 changes contribute to halotropic auxin asymmetry. We also report the formation of “osmotic stress‐induced membrane structures.” These large membrane structures are formed at the plasma membrane shortly after NaCl or sorbitol treatment and have a prolonged presence in a pldζ1 mutant. Taken together, these results show a crucial role for PLDζ1 in both ionic and osmotic stress‐induced auxin carrier dynamics during salt stress.

Genetic Loci Associated with Early Salt Stress Responses of Roots

“…Halotropism is an auxin-dependent root growth away from higher salt concentrations and toward areas with lower salt concentrations. Although previous studies identified auxin transporters to have contributory roles in root halotropic responses (Galvan-Ampudia et al., 2013, Korver et al, 2019, van den Berg et al., 2016), other components of this process remain largely unknown. Here, we screened a set of 333 Arabidopsis accessions using the robust and efficient halotropism assay and associated the observed root phenotypes with SNP markers using GWAS.…”

All Roads Lead to Auxin: Post-translational Regulation of Auxin Transport by Multiple Hormonal Pathways

“…A typical example of such an adaptive response is a rapid bending of roots away from high-salt-containing environments, which is known as halotropism ( Rosquete and Kleine-Vehn, 2013 ). The halotropic bending of roots is a result of tuning PAT that leads to asymmetric redistribution of auxin at the root tip ( Galvan-Ampudia et al., 2013 , van den Berg et al., 2016 , Korver et al., 2020 ). It has been shown that on the side of root that faces a high-salinity environment, clathrin-mediated endocytosis of PIN2 is increased.…”

“…Consequently, as result of the reduced amount of PIN2 at the PM in epidermal cells at the salt exposed side of the root, auxin at the root tip is asymmetrically redistributed, which steers the root away from the salty surroundings ( Galvan-Ampudia et al., 2013 ). Phospholipases (PLDs) and phosphatidic acid (PA), a signaling molecule formed by the action of PLD, have been identified as important molecular players in the regulation of auxin transport mediated through AUX1 and PIN2 in response to salt stress ( Li and Xue, 2007 , Testerink and Munnik, 2011 , Galvan-Ampudia et al., 2013 , Korver et al., 2020 ). Salt-induced stimulation of PLD activity increases the clathrin-mediated endocytosis of PIN2 at the side of the root facing the higher salt concentration, suggesting that PA controls the polar distribution of PIN and auxin polarity during halotropism in plants ( Galvan-Ampudia et al., 2013 ).…”

Halotropism: Phytohormonal Aspects and Potential Applications

“…Phospholipid signaling is also critical in inducing halotropic movement of roots. Phospholipase Dζ1 can modulate the cellular polarity of auxin transport carriers ( Korver et al., 2020 ). Another issue to be answered is the contribution of tissue-specific accumulation of pH-sensing phosphatidic acid to the halotropism ( Li et al., 2019 ).…”