Efficient modulation of photosynthetic apparatus confers desiccation tolerance in the resurrection plant Boea hygrometrica

Plant Cell Physiol. 2017 Nov 1;58(11):1976-1990. doi: 10.1093/pcp/pcx140.

Abstract

Boea hygrometrica (B. hygrometrica) can tolerate severe desiccation and resume photosynthetic activity rapidly upon water availability. However, little is known about the mechanisms by which B. hygrometrica adapts to dehydration and resumes competence upon rehydration. Here we determine how B. hygrometrica deals with oxidative stress, excessive excitation/electron pressures as well as photosynthetic apparatus modulation during dehydration/rehydration. By measuring ROS generation and scavenging efficiency, we found that B. hygrometrica possesses efficient strategies to maintain cellular redox homeostasis. Transmission electron microscopy (TEM) analysis revealed a remarkable alteration of chloroplast architecture and plastoglobules (PGs) accumulation during dehydration/rehydration. Pulse-amplitude modulated (PAM) chlorophyll fluorescence measurements, P700 redox assay as well as chlorophyll fluorescence emission spectra analysis on leaves of B. hygrometrica during dehydration/rehydration were also performed. Results showed that the photochemical activity of PSII as well as photoprotective energy dissipation in PSII undergo gradual inactivation/activation during dehydration/rehydration in B. hygrometrica; PSI activity is relatively induced upon water deficit, and dehydration leads to physical interaction between PSI and LHCII. Furthermore, blue-native polyacrylamide gel electrophoresis (BN-PAGE) and immunoblot analysis revealed that the protein abundance of light harvesting complexes decrease markedly along with internal water deficit to restrict light absorption and attenuate electron transfer, resulting in limited light excitation and repressed photosynthesis. In contrast, many thylakoid proteins remain at a basal level even after full dehydration. Taken together, our study demonstrated that efficient modulation of cellular redox homeostasis and photosynthetic activity confers desiccation tolerance in B. hygrometrica.

Keywords: Boea hygrometrica; Dehydration/rehydration cycle; Desiccation tolerance; Photosynthetic apparatus and activity; Redox homeostasis; Resurrection plant; Thylakoid proteins.

MeSH terms

  • Antioxidants / metabolism
  • Chlorophyll / metabolism
  • Chloroplasts / physiology
  • Dehydration
  • Energy Metabolism
  • Homeostasis
  • Light-Harvesting Protein Complexes / metabolism
  • Magnoliopsida / physiology*
  • Photosynthesis / physiology*
  • Photosystem II Protein Complex / metabolism
  • Plant Cells / metabolism
  • Plant Cells / physiology
  • Thylakoids / metabolism
  • Water / metabolism

Substances

  • Antioxidants
  • Light-Harvesting Protein Complexes
  • Photosystem II Protein Complex
  • Water
  • Chlorophyll