Manganese deficiency alters the patterning and development of root hairs in Arabidopsis

Abstract

Manganese (Mn) is the second most prevalent transition metal in the Earth's crust but its availability is often limited due to rapid oxidation and low mobility of the oxidized forms. Acclimation to low Mn availability was studied in Arabidopsis seedlings subjected to Mn deficiency. As reported here, Mn deficiency caused a thorough change in the arrangement and characteristics of the root epidermal cells. A proportion of the extra hairs formed upon Mn deficiency were located in atrichoblast positions, indicative of a post-embryonic reprogramming of the cell fate acquired during embryogenesis. When plants were grown under a light intensity of >50 μmol m−2 s−1 in the presence of manganese root hair elongation was substantially inhibited, whereas Mn-deficient seedlings displayed stimulated root hair development. GeneChip analysis revealed several candidate genes with potential roles in the reprogramming of rhizodermal cells. None of the genes that function in epidermal cell fate specification were affected by Mn deficiency, indicating that the patterning mechanism which controls the differentiation of rhizodermal cells during embryogenesis have been bypassed under Mn-deficient conditions. This assumption is supported by the partial rescue of the hairless cpc mutant by Mn deficiency. Inductively coupled plasma-optical emission spectroscopy (ICP-OES) analysis revealed that, besides the anticipated reduction in Mn concentration, Mn deficiency caused an increase in iron concentration. This increase was associated with a decreased transcript level of the iron transporter IRT1, indicative of a more efficient transport of iron in the absence of Mn.

Systems-wide analysis of manganese deficiency-induced changes in gene activity of Arabidopsis roots

“…Manganese deficiency was shown to increase root hair length and density, probably to compensate for the low mobility of Mn1532. Several genes with putative or validated roles in root hair development showed increased expression under Mn-deficient conditions but decreased expression in Fe-deficient plants ( DER1 , AGP14 , FLA9 ).…”

“…Such knowledge is of critical importance for the development of Mn-efficient germplasm with improved Mn acquisition and/or increased resource utilization efficiency. Transcriptome profiling has allowed insights into Mn deficiency-induced changes of gene activity15; however, biological processes are carried out by proteins and it is not clear how much the changes observed at the transcript level impact the proteomic readout. In fact, several studies observed only a moderate level of concordance between transcriptomics and proteomics (reviewed by Vogel and Marcotte16), indicating the necessity of integrative studies that cover disparate omics levels.…”

Manganese in Plants: From Acquisition to Subcellular Allocation

“…This suggests that the use of the cellular Mn pool for Mn-requiring metabolic reactions under low Mn conditions is variable among photosynthetic organisms. In roots, an increase in the frequency of root hairs can be observed under Mn deficiency (Yang et al, 2008). If the deficiency becomes more severe, root tips may develop serious necrosis (Yamaji et al, 2013).…”

Elevated Phosphorus Impedes Manganese Acquisition by Barley Plants

“…Both P and Mn ions are rather immobile in soils implying that factors such as root length and root architecture, together with rhizosphere processes, have a major impact on their plant availability (Gahoonia and Nielsen, 1997; Gherardi and Rengel, 2004; Raghothama and Karthikeyan, 2005). The presence of Mn substantially inhibited root hair elongation in Arabidopsis , whereas Mn-deficient seedlings displayed stimulated root hair development (Yang et al, 2008). Also P starvation increases the number of lateral roots and root hair abundance (Gahoonia et al, 1997; Zhu et al, 2010; Miura et al, 2011).…”