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

ABSTRACT: 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.

SUBMITTER: de la Fuente C

PROVIDER: S-EPMC10945517 | biostudies-literature | 2024 Jan

REPOSITORIES: biostudies-literature

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

de la Fuente Carla C Grondin Alexandre A Sine Bassirou B Debieu Marilyne M Belin Christophe C Hajjarpoor Amir A Atkinson Jonathan A JA Passot Sixtine S Salson Marine M Orjuela Julie J Tranchant-Dubreuil Christine C Brossier Jean-Rémy JR Steffen Maxime M Morgado Charlotte C Dinh Hang Ngan HN Pandey Bipin K BK Darmau Julie J Champion Antony A Petitot Anne-Sophie AS Barrachina Celia C Pratlong Marine M Mounier Thibault T Nakombo-Gbassault Princia P Gantet Pascal P Gangashetty Prakash P Guedon Yann Y Vadez Vincent V Reichheld Jean-Philippe JP Bennett Malcolm J MJ Kane Ndjido Ardo NA Guyomarc'h Soazig S Wells Darren M DM Vigouroux Yves Y Laplaze Laurent L

eLife 20240131

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 wa ...[more]

PMID: 38294329

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Project description:Pearl millet (Pennisetum glaucum (L.)) is a vital cereal crop renowned for its ability to thrive in challenging environmental conditions; however, the molecular mechanisms governing its salt stress tolerance remain poorly understood. To address this gap, next-generation RNA sequencing was conducted to compare gene expression patterns in pearl millet seedlings exposed to salt stress with those grown under normal conditions. Our RNA sequencing analysis focused on shoots from 13-day-old pearl millet plants subjected to either salinity stress (150 mmol of NaCl for 3 days) or thermal stress (50°C for 60 s). Of 36,041 genes examined, 17,271 genes with fold changes ranging from 2.2 to 19.6 were successfully identified. Specifically, 2388 genes were differentially upregulated in response to heat stress, whereas 4327 genes were downregulated. Under salt stress conditions, 2013 genes were upregulated and 4221 genes were downregulated. Transcriptomic analysis revealed four common abiotic KEGG pathways that play crucial roles in the response of pearl millet to salt and heat stress: phenylpropanoid biosynthesis, photosynthesis-antenna proteins, photosynthesis, and plant hormone signal transduction. These metabolic pathways are necessary for pearl millet to withstand and adapt to abiotic stresses caused by salt and heat. Moreover, the pearl millet shoot heat stress group showed specific transcriptomics related to KEEG metabolic pathways such as cytochrome P450, cutin, suberine, and wax biosynthesis, zeatin biosynthesis, crocin biosynthesis, ginsenoside biosynthesis, saponin biosynthesis, and biosynthesis of various plant secondary metabolites. In contrast, pearl millet shoots exposed to salinity stress exhibited transcriptomic changes associated with KEEG metabolic pathways related to carbon fixation in photosynthetic organisms, mismatch repair, and nitrogen metabolism. Our findings underscore the remarkable cross-tolerance of pearl millet to simultaneous salt and heat stress, elucidated through the activation of shared abiotic KEGG pathways. This study emphasizes the pivotal role of transcriptomics analysis in unraveling the molecular responses of pearl millet under abiotic stress conditions.

Project description:A pearl millet inbred germplasm association panel (PMiGAP) comprising 250 inbred lines, representative of cultivated germplasm from Africa and Asia, elite improved open-pollinated cultivars, hybrid parental inbreds and inbred mapping population parents, was recently established. This study presents the first report of genetic diversity in PMiGAP and its exploitation for association mapping of drought tolerance traits. For diversity and genetic structure analysis, PMiGAP was genotyped with 37 SSR and CISP markers representing all seven linkage groups. For association analysis, it was phenotyped for yield and yield components and morpho-physiological traits under both well-watered and drought conditions, and genotyped with SNPs and InDels from seventeen genes underlying a major validated drought tolerance (DT) QTL. The average gene diversity in PMiGAP was 0.54. The STRUCTURE analysis revealed six subpopulations within PMiGAP. Significant associations were obtained for 22 SNPs and 3 InDels from 13 genes under different treatments. Seven SNPs associations from 5 genes were common under irrigated and one of the drought stress treatments. Most significantly, an important SNP in putative acetyl CoA carboxylase gene showed constitutive association with grain yield, grain harvest index and panicle yield under all treatments. An InDel in putative chlorophyll a/b binding protein gene was significantly associated with both stay-green and grain yield traits under drought stress. This can be used as a functional marker for selecting high yielding genotypes with 'stay green' phenotype under drought stress. The present study identified useful marker-trait associations of important agronomics traits under irrigated and drought stress conditions with genes underlying a major validated DT-QTL in pearl millet. Results suggest that PMiGAP is a useful panel for association mapping. Expression patterns of genes also shed light on some physiological mechanisms underlying pearl millet drought tolerance.

Project description:Water deficit stress at the early stage of development is one of the main factors limiting pearl millet production. One practice to counteract this limitation would be to resort to the application of hormones to stimulate plant growth and development at critical stages. Exogenous methyl jasmonate (MeJA) can improve drought tolerance by modulating signaling, metabolism, and photosynthesis pathways, therefore, we assumed that can occur in pearl millet during the early stage of development. To decipher the molecular mechanisms controlling these pathways, RNAseq was conducted in two pearl millet genotypes, drought-sensitive SosatC88 and drought-tolerant Souna3, in response to 200 μM of MeJA. Pairwise comparison between the MeJA-treated and non-treated plants revealed 3270 differentially expressed genes (DEGs) among 20,783 transcripts in SosatC88 and 127 DEGs out of 20,496 transcripts in Souna3. Gene ontology (GO) classification assigned most regulated DEGs in SosatC88 to heme binding, oxidation-reduction process, response to oxidative stress and membrane, and in Souna3 to terpene synthase activity, lyase activity, magnesium ion binding, and thylakoid. The Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis reveals that DEGs in SosatC88 are related to the oxidation-reduction process, the biosynthesis of other secondary metabolites, the signal transduction, and the metabolism of terpenoids, while in Souna3, DEGs are related to the metabolism of terpenoids and the energy metabolism. Two genes encoding a diterpenoid biosynthesis-related (Pgl_GLEAN_10009413) and a Glutathione S transferase T3 (Pgl_GLEAN_10034098) were contra-regulated between SosatC88 and Souna3. Additionally, five random genes differentially expressed by RNAseq were validated using qPCR, therefore, they are potential targets for the development of novel strategies breeding schemes for plant growth under water deficit stress. These insights into the molecular mechanisms of pearl millet genotype tolerance at the early stage of development contribute to the understanding of the role of hormones in adaptation to drought-prone environments.

Project description:Pearl millet [Pennisetum glaucum (L) R. Br.] is an important cereal crop of the semiarid tropics, which can withstand prolonged drought and heat stress. Considering an active involvement of the aquaporin (AQP) genes in water transport and desiccation tolerance besides several basic functions, their potential role in abiotic stress tolerance was systematically characterized and functionally validated. A total of 34 AQP genes from P. glaucum were identified and categorized into four subfamilies, viz., plasma membrane intrinsic proteins (PIPs), tonoplast intrinsic proteins (TIPs), nodulin-26-like intrinsic proteins (NIPs), and small basic intrinsic proteins (SIPs). Sequence analysis revealed that PgAQPs have conserved characters of AQP genes with a closer relationship to sorghum. The PgAQPs were expressed differentially under high vapor pressure deficit (VPD) and progressive drought stresses where the PgPIP2;6 gene showed significant expression under high VPD and drought stress. Transgenic tobacco plants were developed by heterologous expression of the PgPIP2;6 gene and functionally characterized under different abiotic stresses to further unravel their role. Transgenic tobacco plants in the T2 generations displayed restricted transpiration and low root exudation rates in low- and high-VPD conditions. Under progressive drought stress, wild-type (WT) plants showed a quick or faster decline of soil moisture than transgenics. While under heat stress, PgPIP2;6 transgenics showed better adaptation to heat (40°C) with high canopy temperature depression (CTD) and low transpiration; under low-temperature stress, they displayed lower transpiration than their non-transgenic counterparts. Cumulatively, lower transpiration rate (Tr), low root exudation rate, declined transpiration, elevated CTD, and lower transpiration indicate that PgPIP2;6 plays a role under abiotic stress tolerance. Since the PgPIP2;6 transgenic plants exhibited better adaptation against major abiotic stresses such as drought, high VPD, heat, and cold stresses by virtue of enhanced transpiration efficiency, it has the potential to engineer abiotic stress tolerance for sustained growth and productivity of crops.

Dataset Information

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

Publications

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

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