The Synergistic Responses of Different Photoprotective Pathways in Dwarf Bamboo (Fargesia rufa) to Drought and Subsequent Rewatering

Abstract

Dwarf bamboo-dominated forests are often subjected to temporary periods of drought due to rising air temperature and decreasing rainfall. Nevertheless, the relationship among CO₂ assimilation, photoprotective pathways and metabolism of reactive oxygen species (ROS) remains unexplored in bamboo species. Changes in leaf gas exchange, chlorophyll fluorescence, energy partitioning, antioxidative system and compounds related to ROS metabolism in Fargesia rufa plants subjected to drought and subsequent rewatering were analyzed. Drought resulted in a reversible inhibition of photochemistry, particularly net CO₂ assimilation, and lipid peroxidation due to ROS accumulation. Meanwhile, photoprotective pathways, including the water-water cycle (especially for moderate drought), and adjustment in antenna pigments, thermal dissipation and antioxidative defense capacity at organelle levels (especially for severe drought), were up-regulated at the stress phase. Conversely, photorespiration was down-regulated after drought stress. As a result, rewatering restored most of the photochemical activity under drought, especially moderate drought. Moreover, thermal dissipation under severe drought was still operated for avoiding high ROS levels after rewatering. Therefore, the synergistic function of these photoprotective pathways except photorespiration can protect the photosynthetic apparatus from oxidative damage in response to varying intensities of drought stress when CO₂ assimilation is restricted. This is helpful for the gradual recovery of photosynthetic capacity after rewatering. Thus, F. rufa plants can withstand drought and is capable of survival in such environment.

Highlights: 1. The effects of drought and subsequent rewatering on Fargesia rufa were studied.2. Drought resulted in a reversible inhibition of photochemistry.3. Photoprotective pathways except photorespiration were up-regulated at the drought phase.4. Rewatering rapidly restored photochemical activity, especially under moderate drought.5. Fargesia rufa plant is capable of resisting and surviving drought environment.

Keywords: CO2 assimilation; antioxidative defense system; energy partitioning; rewatering; the water–water cycle; thermal dissipation.

FIGURE 1

Changes in energy dissipation flux via different pathways of Fargesia rufa plants under drought and rewatering. (A) energy flux via linear electron transport in PSII (J_PSII), (B) energy flux viaΔpH- and xanthophyll-mediated thermal dissipation (J_NPQ), and (C) energy flux via fluorescence and constitutive thermal dissipation (J_f,D). Well-watered (WW, open bars), moderate drought (MD, gray bars), and severe drought (SD, closed bars). Data are the means of four replicates with SE shown by vertical bars. Different letters within the same stage indicate significant differences (P < 0.05) according to Duncan’s test.

FIGURE 2

Changes in the flux of electron transport via different proportions of linear electron transport in PSII (J_PSII) of F. rufa plants under drought and rewatering. (A) electron flux for photosynthetic carbon reduction J_c, (B) electron flux for photorespiratory carbon oxidation J_o, (C) O₂-dependent alternative electron flux (O₂-dependent J_a), and (D) O₂-independent alternative electron flux (O₂-independent J_a). Well-watered (WW, open bars), moderate drought (MD, gray bars), and severe drought (SD, closed bars). Data are the means of four replicates with SE shown by vertical bars. Different letters within the same stage indicate significant differences (P < 0.05) according to Duncan’s test.

FIGURE 3

Changes in reactive oxygen species (ROS) and lipid peroxidation of F. rufa plants under drought and rewatering. (A) superoxide anion (${\mathrm{O}}_{\mathrm{2}}^{\mathrm{•}\mathrm{-}}$) producing rate, (B) hydrogen peroxide (H₂O₂), and (C) lipid peroxidation (MDA content). Well-watered (WW, open bars), moderate drought (MD, gray bars), and severe drought (SD, closed bars). Data are the means of four replicates with SE shown by vertical bars. Different letters within the same stage indicate significant differences (P < 0.05) according to Duncan’s test.

FIGURE 4

Changes in the activities of antioxidative enzymes in chloroplasts (A), mitochondria (B), and cytosol (C) from F. rufa leaves under drought and rewatering. Well-watered (WW, open bars), moderate drought (MD, gray bars), and severe drought (SD, closed bars). Data are the means of four replicates with SE shown by vertical bars. Different letters within the same stage indicate significant differences (P < 0.05) according to Duncan’s test.

FIGURE 5

Relationship between net CO₂ assimilation (P_n) and different energy partitioning processes in F. rufa leaves under drought and rewatering. The regression lines are: (A) y = 7.31x + 29.90, (B) y = –16.51x + 207.48, (C) y = 8.87x + 101.29, (D) y = 7.06x – 3.30, (E) y = 3.29x – 3.29, (F) y = –3.04x + 36.49 (for drought); and (A) y = 1.92x + 52.98, (B) y = –9.36x + 181.61, (C) y = 3.47x + 124.58, (D) y = 2.57x + 19.78, (E) y = 0.15x + 12.41, (F) y = –0.07x + 17.90 (for rewatering). Data are measured values of four replicates per treatment at the same stage (error bars are omitted for clarity). The solid lines represent the best-fit linear regressions: ^∗P < 0.05; ^∗∗∗P < 0.001; ns, not significant.

FIGURE 6

Relationship between lipid peroxidation (MDA) and different energy partitioning processes in F. rufa leaves under drought and rewatering. The regression lines are: (A) y = –12.31x + 92.98, (B) y = 26.33x + 69.35, (C) y = –13.46x + 173.50, (D) y = –9.60x + 50.89, (E) y = –4.03x + 20.69, (F) y = 1.32x + 21.40 (for drought); and (A) y = –2.17x + 66.90, (B) y = 12.19x + 109.43, (C) y = –6.84x + 157.44, (D) y = –1.82x + 35.60, (E) y = –1.04x + 15.79, (F) y = 0.61x + 16.00 (for rewatering). Data are measured values of four replicates per treatment at the same stage (error bars are omitted for clarity). The solid lines represent the best-fit linear regressions: ^∗∗P < 0.01; ^∗∗∗P < 0.001; ns, not significant.