Association of jasmonic acid priming with multiple defense mechanisms in wheat plants under high salt stress

Abstract

Salinity is a global conundrum that negatively affects various biometrics of agricultural crops. Jasmonic acid (JA) is a phytohormone that reinforces multilayered defense strategies against abiotic stress, including salinity. This study investigated the effect of JA (60 μM) on two wheat cultivars, namely ZM9 and YM25, exposed to NaCl (14.50 dSm^-1) during two consecutive growing seasons. Morphologically, plants primed with JA enhanced the vegetative growth and yield components. The improvement of growth by JA priming is associated with increased photosynthetic pigments, stomatal conductance, intercellular CO₂, maximal photosystem II efficiency, and transpiration rate of the stressed plants. Furthermore, wheat cultivars primed with JA showed a reduction in the swelling of the chloroplast, recovery of the disintegrated thylakoids grana, and increased plastoglobuli numbers compared to saline-treated plants. JA prevented dehydration of leaves by increasing relative water content and water use efficiency via reducing water and osmotic potential using proline as an osmoticum. There was a reduction in sodium (Na⁺) and increased potassium (K⁺) contents, indicating a significant role of JA priming in ionic homeostasis, which was associated with induction of the transporters, viz., SOS1, NHX2, and HVP1. Exogenously applied JA mitigated the inhibitory effect of salt stress in plants by increasing the endogenous levels of cytokinins and indole acetic acid, and reducing the abscisic acid (ABA) contents. In addition, the oxidative stress caused by increasing hydrogen peroxide in salt-stressed plants was restrained by JA, which was associated with increased α-tocopherol, phenolics, and flavonoids levels and triggered the activities of superoxide dismutase and ascorbate peroxidase activity. This increase in phenolics and flavonoids could be explained by the induction of phenylalanine ammonia-lyase activity. The results suggest that JA plays a key role at the morphological, biochemical, and genetic levels of stressed and non-stressed wheat plants which is reflected in yield attributes. Hierarchical cluster analysis and principal component analyses showed that salt sensitivity was associated with the increments of Na⁺, hydrogen peroxide, and ABA contents. The regulatory role of JA under salinity stress was interlinked with increased JA level which consequentially improved ion transporting, osmoregulation, and antioxidant defense.

Keywords: Na+ transporter-related gene expression; jasmonic acid; nutrient homeostasis; salinity; wheat.

Figure 1

Effects of JA priming on water potential (A), osmotic potential (B), relative water content [RWC, (C)], water use effciency [WUE, (D)] of two wheat cultivars Mai9 (ZM9, salt-sensitive) and Yang Mai25 (YM25, salt-tolerant) under control and salinity stress conditions during two consecutive growing seasons 2019 and 2020. Means sharing the same letters, for a parameter during a year, do not differ significantly at P ≤ 0.05 among the studied factors. Ck, control; S, salt treatment; JA, jasmonic acid.

Figure 2

Effects of JA priming on the production of reactive oxygen species (H₂O₂) in the shoot (A) and root (B); SOD in the shoot (C) and root (D); APX in the shoot (E) and root (F); PAL in the shoot (G) and root (H) of two wheat cultivars Mai9 (ZM9, salt-sensitive) and Yang Mai25 (YM25, salt-tolerant) under control and salinity stress conditions during two consecutive growing seasons 2019 and 2020. Means sharing the same letters, for a parameter during a year, do not differ significantly at P ≤ 0.05 among the studied factors. SOD, superoxide dismutase; APX, ascorbate peroxidase; PAL, phenylalanine ammonia-lyase; Ck, control; S, salt treatment; JA, jasmonic acid.

Figure 3

Effects of JA priming on flavonoids in the shoot (A) and root (B); total phenols in the shoot (C) and root (D); tocopherol in the shoot (E) and root (F); proline in the shoot (G) and root (H) of two wheat cultivars Mai9 (ZM9, salt-sensitive) and Yang Mai25 (YM25, salt-tolerant) under control and salinity stress conditions during two consecutive growing seasons 2019 and 2020. Means sharing the same letters, for a parameter during a year, do not differ significantly at P ≤ 0.05 among the studied factors. Ck, control; S, salt treatment; JA, jasmonic acid.

Figure 4

Effects of JA priming on cytokinins in the shoot (A) and root (B); IAA in the shoot (C) and root (D); JA in the shoot (E) and root (F); ABA in the shoot (G) and root (H) of two wheat cultivars Mai9 (ZM9, salt-sensitive) and Yang Mai25 (YM25, salt-tolerant) under control and salinity stress conditions during two consecutive growing seasons 2019 and 2020. Means sharing the same letters, for a parameter during a year, do not differ significantly at P ≤ 0.05 among the studied factors. IAA, indole acetic acid; JA, jasmonic acid; ABA, abscisic acid; Ck, control; S, salt treatment.

Figure 5

Effects of JA priming on the relative expression of SOS1, NHX2, and HVP1 in leaf blade [(A–C) respectively], in leaf sheath [(D–F) respectively], in stem [(G–I) respectively], and in the root [(J–L) respectively] of two wheat cultivars Mai9 (ZM9, salt-sensitive) and Yang Mai25 (YM25, salt-tolerant) under control and salinity stress conditions during two consecutive growing seasons 2019 and 2020. Means sharing the same letters, for a parameter during a year, do not differ significantly at P ≤ 0.05 among the studied factors. Ck, control; S, salt treatment; JA, jasmonic acid.

Figure 6

Effect of JA priming on Spike /m² (A), grains/spike (B), and weight of 100 grains [g (C)]; the ultrastructure of the leaf of two wheat cultivars Mai9 (ZM9, salt-sensitive) and Yang Mai25 (YM25, salt-tolerant) under salinity stress, CK [without priming under normal conditions in YM25 (D) and ZM9 (G)]; S1 [exposed to salinity without JA priming in YM25 (E) and ZM9 (H)]; JA priming+S1 [exposed to salinity with JA priming in YM25 (F) and ZM9 (I)].

Figure 7

Cluster analysis showing data correlation clustered the metabolic activities to five clusters; Group A) included ABA (shoot and root), H₂O₂ (shoot and root), Na⁺ content (root, shoot, blade, and sheath), Group B) included IAA (shoot and root), cytokinins (shoot and root), and K+ (root, stem, blade, and sheath), Group C) included JA (shoot and root), PAL (shoot and root), proline (shoot and root), and SOD activity of roots, Group D) included the expression of genes HVP1, NHX2, and SOS1 of stem, root, leaf sheath, and leaf blade, as well as the SOD activity in the shoot, and Group E) included APX activity (shoot and root), tocopherol (shoot and root), flavonoids (shoot and root), and total phenol (shoot and root). ABA, abscisic acid; IAA, indole acetic acid; JA, jasmonic acid; PAL, phenylalanine ammonia-lyase; SOD, superoxide dismutase; APX, ascorbate peroxidase.

Figure 8

A principal component analysis (PCA) determines the degree of association within the treatments and variables of two wheat cultivars Mai9 (ZM9, salt-sensitive) and Yang Mai25 (YM25, salt-tolerant) primed with jasmonic acid (JA) and grown under salinity stress.