Glutaredoxin regulation of primary root growth confers early drought stress tolerance in pearl millet

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de la Fuente, Carla | Grondin, Alexandre | Sine, Bassirou | Debieu, Marilyne | Belin, Christophe | Hajjarpoor, Amir | Atkinson, Jonathan, A | Passot, Sixtine | Salson, Marine | Orjuela, Julie | Tranchant-Dubreuil, Christine | Brossier, Jean-Rémy | Steffen, Maxime | Morgado, Charlotte | Dinh, Hang Ngan | Pandey, Bipin, K | Darmau, Julie | Champion, Antony | Petitot, Anne- Sophie | Barrachina, Celia | Pratlong, Marine | Mounier, Thibault | Nakombo-Gbassault, Princia Aurore | Gantet, Pascal | Gangashetty, Prakash | Guédon, Yann | Vadez, Vincent | Reichheld, Jean-Philippe | Bennett, Malcolm, J | Kane, Ndjido, Ardo | Guyomarc’h, Soazig | Wells, Darren, M | Vigouroux, Yves | Laplaze, Laurent

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This article is dedicated to the memory of Yann Guédon (CIRAD).Data availability: Genomic data are available at the National Center for Biotechnology Information (NCBI) under reference number GCA_002174835.2. Genotyping (GBS) data are available in NCBI BioProject under reference number PRJNA492967 (GWAS) and PRJNA769524 (BSA). RNAseq data are available in the Gene Expression Omnibus (GEO) under reference GSE185517. Oxford Nanopore long reads are available on the European Nucleotide Archive (ENA) under reference ERR12178246 and ERR10627707.Field trials data are available at Dryad under reference https://doi.org/10.5061/dryad.qv9s4mwk2.. International audience. Seedling root traits impact plant establishment under challenging environments. Pearl millet is one of the most heat and drought tolerant cereal crops that provides a vital food source across the sub-Saharan Sahel region. Pearl millet’s early root system features a single fast-growing primary root which we hypothesize is an adaptation to the Sahelian climate. Using crop modelling, we demonstrate that early drought stress is an important constraint in agrosystems in the Sahel where pearl millet was domesticated. Furthermore, we show that increased pearl millet primary root growth is correlated with increased early water stress tolerance in field conditions. Genetics including GWAS and QTL approaches identify genomic regions controlling this key root trait. Combining gene expression data, re-sequencing and re- annotation of one of these genomic regions identified a glutaredoxin-encoding gene PgGRXC9 as the candidate stress resilience root growth regulator. Functional characterization of its closest Arabidopsis homolog AtROXY19 revealed a novel role for this glutaredoxin (GRX) gene clade in regulating cell elongation. In summary, our study suggests a conserved function for GRX genes in conferring root cell elongation and enhancing resilience of pearl millet to its Sahelian environment.

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