Local Auxin Sources Orient the Apical-Basal Axis in Arabidopsis Embryos

Abstract

Establishment of the embryonic axis foreshadows the main body axis of adults both in plants and in animals, but underlying mechanisms are considered distinct. Plants utilize directional, cell-to-cell transport of the growth hormone auxin to generate an asymmetric auxin response that specifies the embryonic apical-basal axis. The auxin flow directionality depends on the polarized subcellular localization of PIN-FORMED (PIN) auxin transporters. It remains unknown which mechanisms and spatial cues guide cell polarization and axis orientation in early embryos. Herein, we provide conceptually novel insights into the formation of embryonic axis in Arabidopsis by identifying a crucial role of localized tryptophan-dependent auxin biosynthesis. Local auxin production at the base of young embryos and the accompanying PIN7-mediated auxin flow toward the proembryo are required for the apical auxin response maximum and the specification of apical embryonic structures. Later in embryogenesis, the precisely timed onset of localized apical auxin biosynthesis mediates PIN1 polarization, basal auxin response maximum, and specification of the root pole. Thus, the tight spatiotemporal control of distinct local auxin sources provides a necessary, non-cell-autonomous trigger for the coordinated cell polarization and subsequent apical-basal axis orientation during embryogenesis and, presumably, also for other polarization events during postembryonic plant life.

Cell type-specific transcriptome analysis in the early Arabidopsis thaliana embryo

“…In addition to the already mentioned auxin efflux carrier PIN1, we were also able to detect the auxin biosynthesis genes TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS1 (TAA1, AT1G70560) and YUCCA4 (YUC4, AT5G11320) as well as SHORT INTERNODES (SHI, AT5G66350) and MYB77 (AT3G50060) as being proembryo enriched, which are involved in auxin biosynthesis and signal transduction, respectively (Cheng et al, 2007;Shin et al, 2007;Stepanova et al, 2008;Baylis et al, 2013). Interestingly, suspensor-specific promoter-reporter expression of YUC4 was recently shown at 16-cell stage of embryogenesis (Robert et al, 2013). However, as previous results showed transcript accumulation at later stages only in the proembryo (Cheng et al, 2007) and LCMderived data do not show expression in the suspensor at the globular stage (see GEO GSE11262), the observed suspensor-specific expression of YUC4 might be due to the promoter-reporter construct likely not reflecting the in vivo mRNA distribution.…”

Plant embryogenesis requires AUX/LAX-mediated auxin influx

“…In 16-cell-stage Arabidopsis embryos the PIN1 auxin transporter switches from an apolar to a polar localisation (Friml et al, 2003;Robert et al, 2013;Wabnik et al, 2013). Correspondingly, a directed auxin flow from the future shoot meristem towards the root pole is activated (Friml et al, 2003(Friml et al, , 2004Wabnik et al, 2013).…”

“…Notably, activation of transcriptional signalling pathways of the plant hormone auxin is pivotal for cellular patterning during embryogenesis (Rademacher et al, 2012;Schlereth et al, 2010;Weijers et al, 2006;Yoshida et al, 2014). However, auxins are not synthesized in all cells (Ljung et al, 2005;Petersson et al, 2009;Robert et al, 2013) and are therefore transported from source to sink tissues by specific influx and efflux proteins (Petrásek and Friml, 2009).…”

VPS36-Dependent Multivesicular Bodies Are Critical for Plasmamembrane Protein Turnover and Vacuolar Biogenesis

“…The polarity of auxin movement is mediated by the asymmetric localization of influx and efflux carriers on the plasma membrane, which regulate auxin flow into and out of cells, respectively. Local auxin distribution is determined primarily by a set of efflux carriers known as the PIN-FORMED proteins (PINs) and is critical for the specification of an apical-basal axis and for leaf formation during embryogenesis (Petrásek and Friml, 2009;Robert et al, 2013). PIN1, PIN4, and PIN7 act in concert to produce patterns of embryo development by controlling auxin flow .…”