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Alterations in the root phenylpropanoid pathway and root–shoot vessel system as main determinants of the drought tolerance of a soybean genotype

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Abstract

Climate change increases precipitation variability, particularly in savanna environments. We have used integrative strategies to understand the molecular mechanisms of drought tolerance, which will be crucial for developing improved genotypes. The current study compares the molecular and physiological parameters between the drought-tolerant Embrapa 48 and the sensitive BR16 genotypes. We integrated the root–shoot system’s transcriptome, proteome, and metabolome to understand drought tolerance. The results indicated that Embrapa 48 had a greater capacity for water absorption due to alterations in length and volume. Drought tolerance appears to be ABA-independent, and IAA levels in the leaves partially explain the higher root growth. Proteomic profiles revealed up-regulated proteins involved in glutamine biosynthesis and proteolysis, suggesting osmoprotection and explaining the larger root volume. Dysregulated proteins in the roots belong to the phenylpropanoid pathways. Additionally, PR-like proteins involved in the biosynthesis of phenolics may act to prevent oxidative stress and as a substrate for modifying cell walls. Thus, we concluded that alterations in the root–shoot conductive vessel system are critical in promoting drought tolerance. Moreover, photosynthetic parameters from reciprocal grafting experiments indicated that the root system is more essential than the shoots in the drought tolerance mechanism. Finally, we provided a comprehensive overview of the genetic, molecular, and physiological traits involved in drought tolerance mechanisms.

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The data that support this study will be shared upon reasonable request to the corresponding author.

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Acknowledgements

The authors would like to thank the Núcleo de Análise de Biomoléculas (NuBioMol), the Universidade Federal de Viçosa, MG, Brazil, the Instituto de Biotecnologia Aplicada a Agropecuária (BIOAGRO), the Instituto Nacional de Ciência e Tecnologia em Interações Planta-Praga (INC-TIPP) and the Brazilian Soybean Genome Consortium (GENOSOJA). This work was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo a Pesquisa de Minas Gerais (FAPEMIG) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

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The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Correspondence to Humberto Josué de Oliveira Ramos.

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Supplementary file1 (DOCX 2049 KB)

12298_2023_1307_MOESM2_ESM.docx

Temporal profile of leaf water potential in the morning (ψPLWP) in two soybean genotypes, one sensitive (BR16), and another tolerant (Embrapa 48) during the water deficit assay. Each point represents the mean + standard error (n = 3, where n represents the number of plants), IRR = irrigated, NI = non-irrigated (not irrigated after imposition of stress). (DOCX 49 KB)

12298_2023_1307_MOESM3_ESM.docx

Effect of drought stress on soluble sugar glucose, fructose, sucrose and starch contents. In (A), (C), (E) and (G) for leaves and in (B), (D), (F) and (H) for roots of the soybean genotypes under irrigation and drought (-1.0 MPa) conditions. Bars represent the mean ± standard error (n = 5, where n represents the number of plants). Different capital letters indicate significant differences between means of the same treatment in different genotypes. Lowercase letters show significant differences between means within the same genotype under different treatments (test-t, p <0.05). (DOCX 588 KB)

12298_2023_1307_MOESM4_ESM.docx

Differences in protein abundances of the roots from both genotypes under regular irrigation. Differences in the protein abundances expressed as fold change between the volume (%) of each protein spot of the drought-tolerant genotype Embrapa 48 relative to the sensitive BR16 genotype under normal irrigation conditions. Positive and negative fold change values indicate up- and down-regulation, respectively. Values of fold change for protein spots when presenting only in a genotype or treatment are shown as 10.00 or -10.00, respectively. (DOCX 20 KB)

12298_2023_1307_MOESM5_ESM.docx

Differences in the abundance of proteins in roots from drought-tolerant Embrapa 48 under drought conditions. Protein abundances were expressed as fold change between the volume (%) of each protein spot of the drought-tolerant genotype Embrapa 48 under drought related to normal irrigation conditions. Positive and negative fold change values indicate up- and down-regulation, respectively. Values of fold change for protein spots when presenting only in a genotype or treatment are shown as 10.00 or -10.00, respectively. (DOCX 18 KB)

12298_2023_1307_MOESM6_ESM.docx

Differences in the protein abundances of the roots from both genotypes under drought conditions. Protein abundances were described as fold change between the volume (%) from 2DE profiles of the drought-tolerant genotype Embrapa 48 related to sensitive BR16 under drought conditions. Positive and negative fold change values indicate up- and down-regulation, respectively. Values of fold change for protein spots when presenting only in a genotype or treatment are shown as 10.00 or -10.00, respectively. (DOCX 17 KB)

12298_2023_1307_MOESM7_ESM.docx

Differences in the abundance of the protein spots stained by Pro-Q® Diamond from the roots of both genotypes under regular irrigation. Differences in phosphoprotein abundances are described as fold changes between each phosphoprotein spot's volume (%). Comparations were performed between drought-tolerant genotype Embrapa 48 compared to sensitive BR16 under normal irrigation conditions. Positive and negative fold change values indicate up- and down-regulation, respectively. Values of fold change for protein spots when presenting only in a genotype or treatment are shown as 10.00 or -10.00, respectively. (DOCX 23 KB)

12298_2023_1307_MOESM8_ESM.docx

Differences in the abundance of the protein spots stained by Pro-Q® Diamond from root 2DE profiles of both genotypes under drought conditions. Differences in phosphoprotein abundances are indicated as fold changes between each phosphoprotein spot's volume (%). Differences in phosphoprotein abundances are described as fold changes between each phosphoprotein spot's volume (%). Comparations were performed between the drought-tolerant genotype Embrapa 48 related to sensitive BR16 drought conditions. Positive and negative fold change values indicate up- and down-regulation, respectively. Values of fold change for protein spots when presenting only in a genotype or treatment are shown as 10.00 or -10.00, respectively. (DOCX 21 KB)

12298_2023_1307_MOESM9_ESM.docx

Analysis of 2D Scores Plot by Partial Least Squares Discriminant Analysis (PLS-DA) of the metabolite profiles by LC/MS from soybean leaves. This plot shows the differences in the abundance of the metabolites analyzed by LC-MS in response to treatments. Blue color represents a decrease, and red color an increase. (DOCX 486 KB)

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Coutinho, F.S., Mesquita, R.O., Rodrigues, J.M. et al. Alterations in the root phenylpropanoid pathway and root–shoot vessel system as main determinants of the drought tolerance of a soybean genotype. Physiol Mol Biol Plants 29, 559–577 (2023). https://doi.org/10.1007/s12298-023-01307-7

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