Genetic control of rhizosheath formation in pearl millet

Abstract

The rhizosheath, the layer of soil that adheres strongly to roots, influences water and nutrients acquisition. Pearl millet is a cereal crop that plays a major role for food security in arid regions of sub-Saharan Africa and India. We previously showed that root-adhering soil mass is a heritable trait in pearl millet and that it correlates with changes in rhizosphere microbiota structure and functions. Here, we studied the correlation between root-adhering soil mass and root hair development, root architecture, and symbiosis with arbuscular mycorrhizal fungi and we analysed the genetic control of this trait using genome wide association (GWAS) combined with bulk segregant analysis and gene expression studies. Root-adhering soil mass was weakly correlated only to root hairs traits in pearl millet. Twelve QTLs for rhizosheath formation were identified by GWAS. Bulk segregant analysis on a biparental population validated five of these QTLs. Combining genetics with a comparison of global gene expression in the root tip of contrasted inbred lines revealed candidate genes that might control rhizosheath formation in pearl millet. Our study indicates that rhizosheath formation is under complex genetic control in pearl millet and suggests that it is mainly regulated by root exudation.

Rhizosheath: An adaptive root trait to improve plant tolerance to phosphorus and water deficits?

“…In Sorghum bicolour, the SbMATE (multidrug toxic compound extrusion) involved in root growth processes (Carvalho et al, 2016) secretes organic acid (citrate), which has been hypothesized as a potent stimulator of soil microbial activity (Macias-Benitez et al, 2020). However, a recent study identified 12 potential QTLs may control rhizosheath formation in pearl millet, indicating complex genetic regulation mainly via root exudation (De la fuente Cantó et al, 2022). Therefore, these genes/ QTLs associated with root growth and stress-responsiveness may improve abiotic stress tolerance.…”

“…While limited rhizosheath development of mutants (lacking root hairs) compared to WT plants demonstrates the importance of root hairs in many crop species (Burak et al, 2021), the importance of root hair traits in modifying rhizosheath development of WT plants varied. In a species (pearl millet— Pennisetum glaucum ) with relatively short root hairs (<0.7 mm), root hair length was weakly correlated ( r 2 = 0.05) with rhizosheath development (De la fuente Cantó et al, 2022), but in barley with longer root hairs (0.6−2.5 mm), root hair length was slightly better correlated ( r 2 = 0.16) with rhizosheath development(George et al, 2014). Thus species vary in the importance of root hair traits in determining rhizosheath development, probably mediated by the physical dimensions of root hairs and exudate chemistry.…”

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

“…Genotyping by sequencing of the panel of pearl millet inbred lines provided 392,493 single nucleotide polymorphisms (SNPs) for association, after filtering on quality, with an average density of 2.5 SNPs per 10 kb ( Debieu et al, 2018 ). For the current study, a set of 392,216 SNPs polymorphic for the 122 inbred lines with a phenotype was selected to conduct GWAS ( de la Fuente Cantó et al, 2022 ). GWAS was performed using the ridge latent factor mixed model (LFMM) algorithm ( Caye et al, 2019 ).…”

Unraveling the interplay between root exudates, microbiota, and rhizosheath formation in pearl millet

“…Similar approaches combining metabonomics and metagenomics have been employed in various plant species, including A. thaliana [ 65 , 74 ], Avena barbata [ 78 ], British bluebells [ 79 ], rice [ 80 ], tomato [ 66 ], potato [ 81 ], and poplar [ 82 ] highlighting the role of root exudation in shaping the root/rhizosphere-associated microbiota and their collective impact on soil aggregation. All of these studies mentioned above, as well as many others, have evidenced the effect of the plant through root exudation on the root/rhizosphere-associated microbiota and their combined role in soil aggregation [ 5 , 83 – 89 ], which is under complex genetic control in pearl millet [ 18 ]. In the future, these omics approaches will continue to evolve and improve, particularly in terms of statistical and bioinformatics analysis [ 90 – 92 ], and combined with more complementary omics tools such as metaproteogenomics, metatranscriptomics and metaproteomics to strengthen the analysis of the plant-soil-microbiota continuum and shed light on this black box [ 82 , 93 – 96 ].…”

“…However, deeper insights into soil–plant-microbiota interactions in the root environment can unlock new avenues for sustainable improvement of pearl millet production [ 15 , 16 ]. The formation of the rhizosheath in pearl millet is genetically controlled and primarily regulated by root exudates [ 17 , 18 ].…”