Glutaredoxin regulation of primary root growth is associated with early drought stress tolerance in pearl millet

• Published in: eLife 2024-01, Vol.12
• Main Authors: 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, Gantet, Pascal, Gangashetty, Prakash, Guedon, Yann, Vadez, Vincent, Reichheld, Jean-Philippe, Bennett, Malcolm J, Kane, Ndjido Ardo, Guyomarc'h, Soazig, Wells, Darren M, Vigouroux, Yves, Laplaze, Laurent
• Format: Article
• Language: English
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.86169.3

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 modeling, 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 genome-wide association study and quantitative trait loci (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. Pearl millet is a staple food for over 90 million people living in regions of Africa and India that typically experience high temperatures and little rainfall. It was domesticated about 4,500 years ago in the Sahel region of West Africa and is one of the most heat and drought tolerant cereal crops worldwide. In most plants, organs known as roots absorb water and essential nutrients from the soil. Young pearl millet plants develop a fast-growing primary root, but it is unclear how this unique feature helps the crop to grow in hot and dry conditions. Using weather data collected from the Sahel over a 20-year period, Fuente, Grondin et al. predicted by modelling that early drought stress is the major factor limiting pearl millet growth and yield in this region. Field experiments found that plants with primary roots that grow faster within soil were better at tolerating early drought than those with slower growing roots. Further work using genetic approaches revealed that a gene known as PgGRXC9 promotes the growth of the primary root. To better understand how this gene works, the team examined a very similar gene in a well-studied m