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Changes induced by lead in root system architecture of Arabidopsis seedlings are mediated by PDR2-LPR1/2 phosphate dependent way

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Abstract

As sessile organisms, plants respond to changing environments modulating their genetic expression, metabolism and postembryonic developmental program (PDP) to adapt. Among environmental stressor, lead (Pb) is one of the most hazardous pollutants which limits crop productivity. Here, we describe in detail the effects of a wide range of concentrations of Pb on growth and development and a possible convergence with phosphate (Pi) starvation response. We found that the response to Pb presents a biphasic curve dose response in biomass accumulation: below 400 µM show a stimulatory effect meanwhile at Pb doses up to 600 µM effects are inhibitory. We found that +Pb (800 µM) modifies root system architecture (RSA) and induces acidification media, according to in silico ion interaction, in the growing medium Pb and Pi coprecipitate and plants grow in both Pi deficiency and Pb stress at the same time, however in spite of seedlings are under Pi starvation AtPT2 expression are Pb downregulated indicating that in addition to Pi starvation stress, Pb regulates physiological responses in root system. Using the mutants stop1, lpr1/2 and lpi3, which are affected in Pi starvation response, we found that changes in RSA by +Pb is genetically regulated and there are shared pathways with Pi starvation response mediated by PDR2-LPR1/2 and LPI3 pathways since lpr1/2 and lpi3 mutants are insensitive to +Pb and Pi starvation. Taking together, these results indicate that similar changes in RSA induced by independent environmental stimuli +Pb and Pi starvation are due to similar mediated response by PDR2-LPR1/2 pathway.

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Acknowledgements

We thank to Laboratorio de Biología del Desarrollo Vegetal directed by José López Bucio for kindly providing us mutant seeds. We thank to León Francisco Ruíz-Herrera for confocal microscopy photography.

Funding

Acknowledge to Consejo Nacional de Ciencia y Tecnología for financial support with: Ciencia Básica CB-2010-01 000000000156851 “Búsqueda de los componentes moleculares que participan en la respuesta de Arabidopsis thaliana a la presencia de metales pesados” and scholarship 331963.

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Correspondence to Lenin Sánchez-Calderón.

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10534_2021_299_MOESM1_ESM.tif

Online Resource 1. Primary root length increases at low concentration of lead. Seedlings were germinated and grown for 12 days after germination on MS 0.1 X supplemented with low concentrations of lead (0 to 200 µM). Primary root length (PRL; a), lateral root density (LRD; b) and representative images (c-e). 0 µM (c), 100 µM (d) and 150 µM of Pb (e). n = 14, graphs and images representative of 2 biological replicas, ± standard error. Different letters indicate statistically different groups. P < 0.05 (TIF 23288 kb)

10534_2021_299_MOESM2_ESM.tif

Online Resource 2. Effect of increasing concentrations of Pb on root system architecture of A. thaliana ecotypes. Columbia-0 (a-c), Wassilewskija (d-f), Landsberg erecta (g-i) and Nossen (j-l). Seedling were germinated and grown on lead supplemented media (0 to 1000 μM of Pb) and primary root length (PRL; a, d, g and j), lateral roots number (LRN; b, e, h and k) and lateral root density (LRD; c, f, i and l) were evaluated at 12 days after germination. n = 12, graphs are representative of 3 biological replicas, ± standard error. Different letters indicate statistically different groups. P < 0.05 (TIF 180731 kb)

10534_2021_299_MOESM3_ESM.tif

Online Resource 3. Plants grown on phosphate starvation (1 µM) or lead (800 µM) show similar phenotype. Seedlings were germinated and grown for 12 days after germination on MS 0.1 X (Control), low Pi (-Pi; 1 µM) or supplemented Pb (+Pb; 800 µM). Primary root length (PRL; a). Lateral root density (LRD; b). Representative images of seedlings grown in MS 0.1 X (c), Pi starvation (d) and Pb supplemented (e) media. n = 16, images representative of 2 biological replicas, ± standard error. Different letters indicate statistically different groups. P < 0.05 (TIF 147266 kb)

10534_2021_299_MOESM4_ESM.tif

Online Resource 4. Lead promotes the biomass accumulation in lpr1/2 and lpi3 Arabidopsis mutants. A. thaliana WT and mutants stop1, lpr1/2 and lpi3 were germinated and grown on control, low Pi (-P; 1 µM) and lead (+Pb; 800 µM) media. Seedlings of 12 days after germination were split off in shoot and root for dry weight measurement. Col-0 (a), lpi3 (b), lpr1/2 (c) and stop1 (d). n=12, graphs representative of 3 biological replicas, ± standard error. Different letters indicate statistically different groups. P < 0.05 (TIF 64700 kb)

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Ortiz-Luevano, R., López-Bucio, J., Martínez-Trujillo, M. et al. Changes induced by lead in root system architecture of Arabidopsis seedlings are mediated by PDR2-LPR1/2 phosphate dependent way. Biometals 34, 603–620 (2021). https://doi.org/10.1007/s10534-021-00299-9

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  • DOI: https://doi.org/10.1007/s10534-021-00299-9

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