Genome-Wide Expression Analysis of Root Tips in Contrasting Rice Genotypes Revealed Novel Candidate Genes for Water Stress Adaptation

Abstract

Root system architecture (RSA) is an important agronomic trait with vital roles in plant productivity under water stress conditions. A deep and branched root system may help plants to avoid water stress by enabling them to acquire more water and nutrient resources. Nevertheless, our knowledge of the genetics and molecular control mechanisms of RSA is still relatively limited. In this study, we analyzed the transcriptome response of root tips to water stress in two well-known genotypes of rice: IR64, a high-yielding lowland genotype, which represents a drought-susceptible and shallow-rooting genotype; and Azucena, a traditional, upland, drought-tolerant and deep-rooting genotype. We collected samples from three zones (Z) of root tip: two consecutive 5 mm sections (Z1 and Z2) and the following next 10 mm section (Z3), which mainly includes meristematic and maturation regions. Our results showed that Z1 of Azucena was enriched for genes involved in cell cycle and division and root growth and development whereas in IR64 root, responses to oxidative stress were strongly enriched. While the expansion of the lateral root system was used as a strategy by both genotypes when facing water shortage, it was more pronounced in Azucena. Our results also suggested that by enhancing meristematic cell wall thickening for insulation purposes as a means of confronting stress, the sensitive IR64 genotype may have reduced its capacity for root elongation to extract water from deeper layers of the soil. Furthermore, several members of gene families such as NAC, AP2/ERF, AUX/IAA, EXPANSIN, WRKY, and MYB emerged as main players in RSA and drought adaptation. We also found that HSP and HSF gene families participated in oxidative stress inhibition in IR64 root tip. Meta-quantitative trait loci (QTL) analysis revealed that 288 differentially expressed genes were colocalized with RSA QTLs previously reported under drought and normal conditions. This finding warrants further research into their possible roles in drought adaptation. Overall, our analyses presented several major molecular differences between Azucena and IR64, which may partly explain their differential root growth responses to water stress. It appears that Azucena avoided water stress through enhancing growth and root exploration to access water, whereas IR64 might mainly rely on cell insulation to maintain water and antioxidant system to withstand stress. We identified a large number of novel RSA and drought associated candidate genes, which should encourage further exploration of their potential to enhance drought adaptation in rice.

Responses of root system architecture to water stress at multiple levels: A meta-analysis of trials under controlled conditions

“…A recent genome-wide association study (GWAS) on the roots of two contrasting rice varieties under drought revealed 288 differentially expressed genes from the families of NAC, AP2/ERF, AUX/IAA, EXPANSIN, WRKY, and MYB (Abdirad et al, 2022). This finding warrants further research into verifying the roles of these genes in the differential RSA responses to water stress as one variety enhanced growth and root exploration to access water to avoid water deficit, whereas the other relied on cell insulation to maintain water and antioxidant system to withstand water stress (Abdirad et al, 2022).…”

Comparative metabolomics of root-tips reveals distinct metabolic pathways conferring drought tolerance in contrasting genotypes of rice

“…Potential marker genes involved in sugar metabolism, root growth and elongation were identified in our previous transcriptome studies on two rice genotypes with different drought tolerance [ 31 , 32 ]. Thirteen genes were selected as candidate markers, and their expression levels were measured by qRT-PCR in the roots of the two genotypes grown under control and drought stress conditions.…”

“…Consistent with our previous miRNA-seq and mRNA reports [ 31 , 32 ], 13 genes involved in root growth and elongation and regulation of root primary metabolism were selected. Total RNA isolation was done using the TRIzol reagent (BioBasic-BS410A, Canada) as per the manufacturer’s guidelines.…”

Molecular Characterization and Drought Resistance of GmNAC3 Transcription Factor in Glycine max (L.) Merr.

“…Additionally, a previous GWAS study revealed the wheat NAC gene (i.e., TaNAC071-A ) was closely associated with drought tolerance, i.e., the knockdown of TaNAC071-A attenuated drought tolerance of wheat, whereas its overexpression significantly enhanced drought tolerance through improved water-use efficiency and increased expression of stress-responsive genes [ 79 ]. Another genome-wide expression analysis in rice revealed novel candidate genes involved in water stress adaptation, including members in the families of NAC, AP2/ERF, WRKY, and MYB playing important roles in drought adaptation [ 80 ]. These results indicated that the identification of these QTLs and genes involved in drought tolerance would significantly facilitate the molecular breeding of drought tolerant soybean plants.…”