Jasmonic Acid Is Required for Plant Acclimation to a Combination of High Light and Heat Stress

Abstract

In the field, plants experience high light (HL) intensities that are often accompanied by elevated temperatures. Such conditions are a serious threat to agriculture production, because photosynthesis is highly sensitive to both HL intensities and high-temperature stress. One of the potential cellular targets of HL and heat stress (HS) combination is PSII because its degree of photoinhibition depends on the balance between the rate of PSII damage (induced by light stress), and the rate of PSII repair (impaired under HS). Here, we studied the responses of Arabidopsis (Arabidopsis thaliana) plants to a combination of HL and HS (HL+HS) conditions. Combined HL+HS was accompanied by irreversible damage to PSII, decreased D1 (PsbA) protein levels, and an enhanced transcriptional response indicative of PSII repair activation. We further identified several unique aspects of this stress combination that included enhanced accumulation of jasmonic acid (JA) and JA-Ile, elevated expression of over 2,200 different transcripts that are unique to the stress combination (including many that are JA-associated), and distinctive structural changes to chloroplasts. A mutant deficient in JA biosynthesis (allene oxide synthase) displayed enhanced sensitivity to combined HL+HS and further analysis revealed that JA is required for regulating several transcriptional responses unique to the stress combination. Our study reveals that JA plays an important role in the acclimation of plants to a combination of HL+HS.

Figure 1.

A combination of HL+HS is detrimental to plants. A, Representative images of Col plants subjected to HL, HS, and combined HL+HS. Scale bar = 1 cm. B, Φ_PSII immediately after the application of each stress (top) and 24 h after recovery from the stress treatments (bottom). C, F_v/F_m immediately after the application of each stress (top) and 24 h after recovery from the stress treatments (bottom). D, LDI of Col plants after the stress treatments (top) and survival of plants subjected to the different stresses (bottom). Error bars represent sd (n = 30). Values statistically different at P < 0.05 are denoted with different letters.

Figure 2.

Combined HL+HS causes a heat-like stomatal response. Stomatal aperture (left), surface leaf temperature (middle), and leaf RWC (right) of Col plants subjected to HL, HS, and combined HL+HS. Error bars represent sd (n = 600 for stomatal aperture; n = 50 for leaf temperature and RWC). Values statistically different at P < 0.05 are denoted with different letters. Representative stomatal images are shown on the left. Scale bar in stomatal images = 10 μm.

Figure 3.

Combined HL+HS is accompanied by a unique transcriptomic response. A, Venn diagrams showing the overlap among the upregulated (top) and downregulated (bottom) transcripts in each of the different stress treatments (HL, HS, and combined HL+HS). B, GO annotation of transcripts specifically upregulated in leaves of Arabidopsis in response to HL+HS (numbers above each bar represent P value for statistical significance).

Figure 4.

Differential expression of transcriptional regulators during the stress combination. Heat maps showing the response of different transcriptional regulators in HL, HS, and combined HL+HS conditions (relative to CT). A, HSF family. B, AP2/EREBP family. C, MYB family.

Figure 5.

Enhanced expression of transcripts encoding PSII and PSII repair proteins during combined HL+HS is accompanied by a decrease in D1. A, Heat map showing changes in expression of transcripts encoding proteins of the photosynthetic apparatus in Col leaves in response to HL, HS, and the combination of HL+HS. B, Accumulation of D1 proteins in response to each stress condition. Error bars represent sd (n = 3). Values statistically different at P < 0.05 are denoted with different letters. C, Heat map showing changes in the expression of transcripts encoding proteins involved in the D1 turnover in Col leaves in response to each stress.

Figure 6.

Unique structural features of chloroplasts from plants subjected to HL, HS, and combined HL+HS. A, Representative TEM images of chloroplasts of Col plants subjected to the different stresses. Images were taken at different magnification levels. Scale bar = 0.5 or 0.2 μm (as labeled in each image). B, Quantification bar graphs showing structural changes to chloroplasts of plants subjected to the different stresses. At least 100 images, each containing two to four chloroplasts from at least three plants from each treatment, were analyzed. Error bars represent sd. Values statistically different at P < 0.05 are denoted with different letters.

Figure 7.

Levels of H₂O₂, ABA, SA, JA, JA-Ile, and OPDA in Col plants subjected to HL, HS, and combined HL+HS. A, H₂O₂. B, ABA. C, SA. D, JA, JA-Ile, and OPDA. Error bars represent sd (n = 15). Values statistically different at P < 0.05 are denoted with different letters.

Figure 8.

Involvement of JA in the response of plants to combined HL+HS. A, Venn diagram showing the overlap between JA-responsive transcripts and transcripts upregulated in response to combined HL+HS (top), and heat map showing changes in the expression of JA-response transcriptional regulators during HL, HS, and HL+HS (bottom). B, Representative images of aos plants subjected to the different stress treatments. Scale bar = 1 cm. C, Φ_PSII (top) and F_v/F_m (bottom) immediately after the application of each stress in aos plants. D, LDI showing the appearance of aos plants in response to each stress treatment (top) and survival of aos plants subjected to the different stress treatments (bottom). Values statistically different at P < 0.05 are denoted with different letters. E, Relative expression of the transcriptional regulators ZAT6, ZAT10, and MYB15 and the ROS-scavengers APX1 and APX2 in Col and aos plants in response to the different stresses. Error bars represent sd (n = 30). Asterisks denote Student’s t test significance at P < 0.05.