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. 2013 Jan;64(1):253-63.
doi: 10.1093/jxb/ers335. Epub 2012 Nov 26.

Enhanced seed production under prolonged heat stress conditions in Arabidopsis thaliana plants deficient in cytosolic ascorbate peroxidase 2

Nobuhiro Suzuki  1 , Gad Miller, Hiroe Sejima, Jeffery Harper, Ron Mittler
Affiliations

Enhanced seed production under prolonged heat stress conditions in Arabidopsis thaliana plants deficient in cytosolic ascorbate peroxidase 2

Nobuhiro Suzuki et al. J Exp Bot. 2013 Jan.

Abstract

Reactive oxygen species play a key role in the response of plants to abiotic stress conditions. Their level is controlled in Arabidopsis thaliana by a large network of genes that includes the H(2)O(2)-scavenging enzymes cytosolic ascorbate peroxidase (APX) 1 and 2. Although the function of APX1 has been established under different growth conditions, genetic evidence for APX2 function, as well as for the mode of cooperation between APX1 and APX2, is very limited. This study characterized the response of Arabidopsis mutants deficient in APX1, APX2, and APX1/APX2 to heat, salinity, light, and oxidative stresses. The findings reveal that deficiency in APX2 resulted in a decreased tolerance to light stress, as well as an enhanced tolerance to salinity and oxidative stresses. Interestingly, plants lacking APX2 were more sensitive to heat stress at the seedling stage, but more tolerant to heat stress at the reproductive stage. Cooperation between APX1 and APX2 was evident during oxidative stress, but not during light, salinity, or heat stress. The findings demonstrate a role for APX2 in the response of plants to light, heat, salinity, and oxidative stresses. The finding that plants lacking APX2 produced more seeds under prolonged heat stress conditions suggests that redundant mechanisms activated in APX2-deficient plants during heat stress play a key role in the protection of reproductive tissues from heat-related damage. This finding is very important because heat-associated damage to reproductive tissues in different crops is a major cause for yield loss in agriculture production worldwide.

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Figures

Fig. 1.
Fig. 1.
Gene structure and expression of APX1 and APX2 in wild-type plants and the different mutants used in this study. (A) A gene map showing the site of T-DNA insertion into the APX1 or APX2 genes in apx1 or apx2 plants. (B) Expression of APX1 and APX2 in wild-type (WT), apx1, apx2, and apx1/apx2 plants grown under controlled growth conditions (control: 21 °C) or subjected to heat stress (HS: 38 °C, 1h).
Fig. 2.
Fig. 2.
Long-term exposure of wild-type (WT), apx1, apx2, and apx1/apx2 plants to light stress. (A) Photographs of plants grown under controlled growth conditions (control: 50 µmol m–2 s–1) or light stress (HL: 1000 µmol m–2 s–1). Six-day-old plants were subjected to light stress for 14 days. Bar = 5mm. (B) Diameter of plants grown under controlled conditions or subjected to light stress as described in A. (C) Anthocyanin accumulation in plants grown under controlled conditions or subjected to light stress as described in A. Anthocyanin levels were determined from absorbance at 530nm (A530) and 657nm (A657), and calculated as (A530 – 0.25×A657)/fresh weight. Stress treatments and anthocyanin extraction were performed as described in Materials and methods. **, Student’s t-test significant at P < 0.01.
Fig. 3.
Fig. 3.
Steady-state level of transcripts encoding different abiotic stress acclimation and ROS-response proteins in control (WT), apx1, apx2, and apx1/apx2 plants grown under controlled growth conditions (time 0), or subjected to light stress (1000 µmol m–2 s–1) for 0.5, 1, or 3h. Steady-state level of transcripts was determined by RNA gel blots as described in Materials and methods.
Fig. 4.
Fig. 4.
Effect of oxidative stress on H2O2 accumulation and root growth in seedlings of control (WT), apx1, apx2, and apx1/apx2 plants. (A) Accumulation of H2O2 in WT, apx1, apx2, and apx1/apx2 seedlings in the presence or absence of different concentrations of the superoxide-generating compound paraquat. H2O2 was detected using Amplex Red as described in Materials and methods. (B) Root growth of WT, apx1, apx2, and apx1/apx2 seedlings subjected to the same oxidative stress treatment as in A. **, Student’s t-test significant at P < 0.01.
Fig. 5.
Fig. 5.
Effect of salinity stress on H2O2 accumulation and root growth of control (WT), apx1, apx2, and apx1/apx2 plants. (A) Accumulation of H2O2 in WT, apx1, apx2, and apx1/apx2 seedlings in the presence or absence of different concentrations NaCl. H2O2 was detected using Amplex Red as described in Materials and methods. (B) Root growth of WT, apx1, apx2, and apx1/apx2 seedlings subjected to salinity stress. **, Student’s t-test significant at P < 0.01.
Fig. 6.
Fig. 6.
Effect of heat stress on control (WT), apx1, apx2, and apx1/apx2 seedlings. (A) Root growth of WT, apx1, apx2, and apx1/apx2 seedlings under heat stress (38 °C). Five- to six-day-old plants were subjected to 1 or 6h heat stress, followed by a 4-day recovery period. (B) Acquired and basal thermotolerance of WT, apx1, apx2, and apx1/apx2 seedlings. Five-day-old seedlings were directly subjected to heat stress (45 °C) for 2h to measure basal thermotolerance, or treated at 38 °C for 1.5h, allowed to recover for 1h at 21 °C, and subjected to 45 °C for 2h to measure acquired thermotolerance.
Fig. 7.
Fig. 7.
Effect of heat stress on seed production and silique length in control (WT), apx1, apx2, and apx1/apx2 plants. (A) Photographs of representative cleared siliques from WT, apx1, apx2, and apx1/apx2 plants grown under controlled growth conditions (control), or subjected to periodic heat stress at 42 or 45 °C. Bar=5mm (B and C) Graphs showing silique length (B), and number of seeds per silique (C), from WT, apx1, apx2, and apx1/apx2 plants grown under controlled growth conditions (control), or subjected to periodic heat stress at 42 or 45 °C. Siliques were obtained from plants subjected to different temperatures of heat stress (42 and 45 °C) and treated with 80% ethanol to remove chlorophyll as described in Materials and methods. **, Student’s t-test significant at P < 0.01.
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