Auxin and pectin remodeling interplay during rootlet emergence in white lupin

Abstract

Secondary root emergence is a crucial trait that shapes the plants underground system. Virtually every developmental step of root primordium morphogenesis is controlled by auxin. However, how the hormone controls cell separation in primordium-overlaying tissues through wall loosening is poorly understood. Here, we took advantage of white lupin and its spectacular cluster root development to assess the contribution of auxin to this process. We show that auxin positive role on rootlet emergence is associated with an upregulation of cell wall pectin modifying and degrading genes. Downregulation of a pectinolytic enzyme gene expressed in cells surrounding the primordium resulted in delayed emergence. Pectins were demethylesterified in the emergence zone and auxin treatment further enhanced this effect. Additionally, we report specific rhamnogalacturonan-I modifications during cortical cell separation. In conclusion, we propose a model in which auxin has a dual role during rootlet emergence: Firstly, through active pectin demethylesterification and secondly by regulating the expression of cell wall remodeling enzymes.

Modulation of Polar Auxin Transport Identifies the Molecular Determinants of Source-Sink Carbon Relationships and Sink Strength in Poplar

“…Among the upregulated genes, the expression of polygalacturonase (Potri.007G144200) (PGA) was 2.5-fold up-regulated under the AE-condition compared to controls. This gene is involved in the cell wall pectin polymer modification process, enabling lateral root outgrowth (Jobert et al 2021; Peretto et al 1992). Moreover, three transcripts encoding AAA-ATPases (Potri.004G012700: 1.31-fold, Potri.T104100: 1.56-fold, Potri.004G012500: 1.12-fold) were up-regulated in AE-treated roots.…”

“…Sink establishment and maintenance are facilitated by a continuous biosynthesis, deposition, and modification of cell wall polymers that comprise the structural carbohydrates of plants. Auxin regulates cell expansion and cell wall biosynthesis through cell wall modification genes including polygalacturonase (Jobert et al 2021; Peretto et al 1992), expansins, xyloglucan endotransglucosylase (XTH) (Majda and Robert 2018). Polygalacturonase is a pectin remodifying enzyme exclusively expressed under auxin’s influence to loosen the cell walls to facilitate the lateral root emergence process (Jobert et al 2021; Peretto et al 1992).…”

“…Auxin regulates cell expansion and cell wall biosynthesis through cell wall modification genes including polygalacturonase (Jobert et al 2021; Peretto et al 1992), expansins, xyloglucan endotransglucosylase (XTH) (Majda and Robert 2018). Polygalacturonase is a pectin remodifying enzyme exclusively expressed under auxin’s influence to loosen the cell walls to facilitate the lateral root emergence process (Jobert et al 2021; Peretto et al 1992). Interestingly, the gene expression analysis of AE-roots identified a transcript encoding polygalacturonase (Fig.4, supplementary table S3), reaffirming an active lateral root (sink) growth under AE condition as highlighted by our root phenotypic results (Figs 2 and 3).…”

Biochemical characterization of Pectin Methylesterase Inhibitor 3 from Arabidopsis thaliana

“…Pectins are galacturonic acid (GalA) - containing polysaccharides among which the linear polymer homogalacturonan (HG) is the most abundant matrix polysaccharide, for instance representing 20% of the total cell wall polysaccharides, in Arabidopsis thaliana leaves (Zablackis et al, 1995) or even 50% in onion epidermis cells (Wilson et al, 2021). In vivo studies show that the metabolism of HG plays a critical role in the control of cell expansion and plant morphogenesis (Andres-Robin et al, 2018; K. T. Haas et al, 2020; Jobert et al, 2021; Peaucelle et al, 2015, 2008; Phyo et al, 2017; Qi et al, 2017; Stefanowicz et al, 2021; Wachsman et al, 2020) but the underlying mechanisms are still poorly understood.…”

Biochemical Characterization of Pectin Methylesterase Inhibitor 3 from Arabidopsis Thaliana

“…Pectins are galacturonic acid (GalA) -containing polysaccharides among which the linear polymer HG is the most abundant matrix polysaccharide, for instance representing 20% of the total cell wall polysaccharides, in Arabidopsis thaliana leaves (Zablackis et al, 1995) or even 50% in onion epidermis cells (Wilson et al, 2021). In vivo studies show that the metabolism of HG plays a critical role in the control of cell expansion and plant morphogenesis (Andres-Robin et al, 2018;Haas et al, 2020;Jobert et al, 2021;Peaucelle et al, 2015Peaucelle et al, , 2008Phyo et al, 2017;Qi et al, 2017;Stefanowicz et al, 2021;Wachsman et al, 2020), but the underlying mechanisms are still poorly understood.…”