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Plant and Cell Physiology Advance Access originally published online on August 10, 2009
Plant and Cell Physiology 2009 50(10):1736-1749; doi:10.1093/pcp/pcp116
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© The Author 2009. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org

Differential Positioning of C4 Mesophyll and Bundle Sheath Chloroplasts: Aggregative Movement of C4 Mesophyll Chloroplasts in Response to Environmental Stresses

Masahiro Yamada1, Michio Kawasaki2, Tatsuo Sugiyama3, Hiroshi Miyake1 and Mitsutaka Taniguchi1,*

1Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Aichi, 464-8601 Japan
2Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, Aomori, 036-8561 Japan
3Research Institute of Life and Health Sciences, Chubu University, Kasugai, Aichi, 487-8501 Japan

*Corresponding author: E-mail, taniguti{at}agr.nagoya-u.ac.jp; Fax, +81-52-789-4063.


  Abstract

In C4 plants, mesophyll (M) chloroplasts are randomly distributed along the cell walls, while bundle sheath (BS) chloroplasts are typically located in either a centripetal or centrifugal position. We investigated whether these intracellular positions are affected by environmental stresses. When mature leaves of finger millet (Eleusine coracana) were exposed to extremely high intensity light, most M chloroplasts aggregatively re-distributed to the BS side, whereas the intracellular arrangement of BS chloroplasts was unaffected. Compared with the homologous light-avoidance movement of M chloroplasts in C3 plants, it requires extremely high light (3,000–4,000 µmol m–2 s–1) and responds more slowly (distinctive movement observed in 1 h). The high light-induced movement of M chloroplasts was also observed in maize (Zea mays), another C4 species, but with a distinct pattern of redistribution along the sides of anticlinal walls, analogous to C3 plants. The aggregative movement of M chloroplasts occurred at normal light intensities (250–500 µmol m–2 s–1) in response to environmental stresses, such as drought, salinity and hyperosmosis. Moreover, the re-arrangement of M chloroplasts was observed in field-grown C4 plants when exposed to mid-day sunlight, but also under midsummer drought conditions. The migration of M chloroplasts was controlled by actin filaments and also induced in a light-dependent fashion upon incubation with ABA, which may be the physiological signal transducer. Together these results suggest that M and BS cells of C4 plants have different mechanisms controlling intracellular chloroplast positioning, and that the aggregative movement of C4 M chloroplasts is thought to be a protective response under environmental stress conditions.

Keywords: C4 photosynthesis - Chloroplast - Eleusine coracana - Environmental stress - Photo-relocation movement - Zea mays

Abbreviations: BS, bundle sheath; DAPI, 4',6-diamidino-2-phenylindole; DMSO, dimethylsulfoxide; M, mesophyll; ME, malic enzyme.

(Received June 6, 2009; Accepted August 2, 2009)
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