Cellular Auxin Homeostasis under High Temperature Is Regulated through a SORTING NEXIN1–Dependent Endosomal Trafficking Pathway

Abstract

(A.R.).High-temperature-mediated adaptation in plant architecture is linked to the increased synthesis of the phytohormone auxin, which alters cellular auxin homeostasis. The auxin gradient, modulated by cellular auxin homeostasis, plays an important role in regulating the developmental fate of plant organs. Although the signaling mechanism that integrates auxin and high temperature is relatively well understood, the cellular auxin homeostasis mechanism under high temperature is largely unknown. Using the Arabidopsis thaliana root as a model, we demonstrate that under high temperature, roots counterbalance the elevated level of intracellular auxin by promoting shootward auxin efflux in a PIN-FORMED2 (PIN2)-dependent manner. Further analyses revealed that high temperature selectively promotes the retrieval of PIN2 from late endosomes and sorts them to the plasma membrane through an endosomal trafficking pathway dependent on SORTING NEXIN1. Our results demonstrate that recycling endosomal pathway plays an important role in facilitating plants adaptation to increased temperature.

Light Signaling, Root Development, and Plasticity

“…Phyb mutants have been shown to produce fewer lateral roots (Salisbury et al, 2007), and Phyb and Phya single and double mutants have reduced root elongation compared with the wild type (Correll and Kiss, 2005;Silva-Navas et al, 2015). Recently, PhyB has been identified to act as a temperature sensor (Jung et al, 2016;Legris et al, 2016), which is interesting since heat stress is known to lead to increased main root growth (Hanzawa et al, 2013). If this occurs through PhyB signaling has yet to be resolved, but since high temperatures destabilize PhyB and PhyB mutants have reduced root lengths, this may not be likely.…”

Role of SKD1 Regulators LIP5 and IST1-LIKE1 in Endosomal Sorting and Plant Development

“…The localization and endosomal recycling rates of PIN2 depend on auxin and other hormones (Paciorek et al, 2005;Willige et al, 2011;Löfke et al, 2013;Marhavý et al, 2014), light (Laxmi et al, 2008;Wan et al, 2012), temperature (Shibasaki et al, 2009;Hanzawa et al, 2013), cell types (Löfke et al, 2015), and gravity (Abas et al, 2006;Rahman et al, 2010).…”

“…However, the sole increase of PIN2 abundance at the plasma membrane has been shown to enhance root gravitropic response. For example, enhanced gravity root responses have been associated with increased accumulation of PIN2 at the plasma membrane due to (1) enhanced PIN2 endosomal recycling associated with gibberellic acid accumulation (Löfke et al, 2013) or high temperature (Hanzawa et al, 2013); (2) reduced PIN2 endocytosis in ROP6 gain-of-function lines (Chen et al, 2012); and (3) stabilization of PIN2 at the plasma membrane by overexpression of the tonoplast transporter ZINC INDUCED FACILITATOR-LIKE1.1 (Remy et al, 2013). Thus, although it is reasonable to think that enhanced gravitropism in lip5 roots could be due to the combined changes in abundance and localization of many plasma membrane proteins, the over-accumulation of PIN2 at the plasma membrane itself could explain the observed root-tropic responses to gravity.…”

“…As plasma membrane proteins are in continuous endocytic and recycling fluxes through the endomembrane system, the failure to efficiently sequester PIN2 into ILVs would likely affect PIN2 recycling rates as well. The endosomal recycling of PIN2 depends on the retromer proteins SORTIN NEXIN1 and VACUOLAR PROTEIN SORTING29 (Jaillais et al, 2006(Jaillais et al, , 2007Kleine-Vehn et al, 2008;Hanzawa et al, 2013). The rate of PIN2 recycling can be affected by environmental factors.…”

The dynamics of plant plasma membrane proteins: PINs and beyond

“…In mechanistic terms, SNX1 endosomes appear to be recruited to microtubules by direct interaction between retromer and microtubule-associated CLASP, which has been suggested to control cargo recycling to the plasma membrane (Ambrose et al, 2013). SNX1, in particular, appears to control variations in PIN2 degradation in gravistimulated roots and mediates PIN2 retrieval from late endosomes in response to increased temperature, thus linking retromer activity to adaptive growth responses (Jaillais et al, 2006;Kleine-Vehn et al, 2008a;Hanzawa et al, 2013). SNX1 has also been implicated in the recycling of internalized IRT1 from late endosomes to prevent its premature degradation (Ivanov et al, 2014).…”