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. 2023 Jun 21;12(13):2404.
doi: 10.3390/plants12132404.

Integrating Transcriptional, Metabolic, and Physiological Responses to Drought Stress in Ilex paraguariensis Roots

Edgardo H Avico  1 , Raúl M Acevedo  1 , María J Duarte  1 , Acácio Rodrigues Salvador  2 , Adriano Nunes-Nesi  2 , Oscar A Ruiz  3 , Pedro A Sansberro  1
Affiliations

Integrating Transcriptional, Metabolic, and Physiological Responses to Drought Stress in Ilex paraguariensis Roots

Edgardo H Avico et al. Plants (Basel). .

Abstract

The appearance of water stress episodes triggers leaf abscission and decreases Ilex paraguariensis yield. To explore the mechanisms that allow it to overcome dehydration, we investigated how the root gene expression varied between water-stressed and non-stressed plants and how the modulation of gene expression was linked to metabolite composition and physiological status. After water deprivation, 5160 differentially expressed transcripts were obtained through RNA-seq. The functional enrichment of induced transcripts revealed significant transcriptional remodelling of stress-related perception, signalling, transcription, and metabolism. Simultaneously, the induction of the enzyme 9-cis-expoxycarotenoid dioxygenase (NCED) transcripts reflected the central role of the hormone abscisic acid in this response. Consequently, the total content of amino acids and soluble sugars increased, and that of starch decreased. Likewise, osmotic adjustment and radical growth were significantly promoted to preserve cell membranes and water uptake. This study provides a valuable resource for future research to understand the molecular adaptation of I. paraguariensis plants under drought conditions and facilitates the exploration of drought-tolerant candidate genes.

Keywords: Ilex paraguariensis; RNA-seq; drought stress response; root transcriptome.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Effect of severe drought stress (Ψsoil = −2 MPa) on root hair formation. Left: distance of root hair zone formation from the root tip. Bars indicate mean ± SE (n = 10); three asterisks denote p < 0.001 for the t-test. Right: scanning electron microscopy images of the root tips from non-stressed and stressed roots. Bar indicates 200 µm.
Figure 2
Figure 2
KEGG diagram of plant hormone signal transduction in Ilex paraguariensis root subjected to a severe drought stress (Ψsoil = −2 MPa) episode. Green and red indicate increased and decreased expression (FC ≥ 2, FDR < 0.001).
Figure 3
Figure 3
Interaction network of predicted proteins from up-regulated genes. The analysis of functional associations was performed with the A. thaliana database based on information from root RNA-seq data of drought-stressed I. paraguariensis plants. The line width indicates the type and reliability of evidence about the interaction. A confidence value of 0.4 was used. The GO biological process to which the proteins (nodes) of the identified clusters belong is indicated with a key colour: response to osmotic stress (yellow), translation (light blue), response to abscisic acid (light green), proteolysis (brown), response to heat (red), glycolysis/gluconeogenesis (purple), and cell wall (dark green).
Figure 4
Figure 4
Metabolomic profile of I. paraguariensis roots subjected to a severe drought stress (Ψsoil = −2 MPa) episode. Bars represent the mean of three biological replicates ± SD. Values are expressed in absolute or relative terms. Bars with different colours indicate variation in the content of biological compounds between treatments (t-test, p < 0.05). Red and green indicate lower and higher levels than the well-watered control. The white colour indicates no variation. C, non-stressed (Ψsoil ~ −0.04 Mpa); S, stressed (Ψsoil = −2 Mpa) plants. RQ, relative quantity.
Figure 5
Figure 5
Schematic diagram of drought-induced changes in the I. paraguariensis root amino acid metabolism. Bars represent the mean of three biological replicates ± SD. Values are expressed in relative terms to control plant level. Bars with different colours indicate variation in the content of biological compounds between treatments (t-test, p < 0.05). Red and green indicate lower and higher levels than the well-watered control. White colour shows a non-significant difference concerning the well-watered conditions. C, non-stressed (Ψsoil ~ −0.04 MPa); S, stressed (Ψsoil = −2 MPa) plants. RQ, relative quantity.
Figure 6
Figure 6
Ilex paraguariensis response to water shortage. Schematic diagram of the morphological, physiological, and biochemical changes in the whole plant under a severe drought episode. Parameters promoted or repressed in response to the strain are highlighted in green and red, respectively.
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